Plant Breeding Reviews (Janick/Plant Breeding Reviews, Volume 27) || Synteny in the Rosaceae

4

Synteny in the RosaceaePere ArúsDepartment de Genètica Vegetal, Laboratori de Genètica MolecularVegetal, CSIC-IRTACarretera de Cabrils s/n; 08348, Cabrils, Spain

Toshiya YamamotoNational Institute of Fruit Tree ScienceTsukuba, Ibaraki 305-8605, Japan

Elisabeth DirlewangerINRA, Unité de Recherches sur les Espèces Fruitières et la VigneB.P. 81, F-33 883 Villenave d’Ornon cedex, France

Albert G. AbbottDepartment of Genetics, Biochemistry and Life Science Studies,Clemson UniversityClemson, South Carolina 29634, USA

I. INTRODUCTIONII. GENETIC MAPS IN THE MAIN ROSACEAE SPECIES

A. Subfamily Prunoideae1. Subgenus Amygdalus2. Subgenus Prunophora3. Subgenus Cerasus

B. Subfamily Maloideae1. Apple2. Pear

C. Subfamily RosoideaeIII. MAP COMPARISONS

A. Within the Prunus GenusB. Between Apple and PearC. Between Apple and PrunusD. Between Prunus and Arabidopsis

175

04_4453.qxd 10/20/05 3:06 PM Page 175

Plant Breeding Reviews, Volume 27 Edited by Jules Janick

© 2006 John Wiley & Sons, Inc. ISBN: 978-0-471-73213-6

IV. OTHER GENETIC RESOURCES OF INTEREST FOR MAP COMPARISONA. The Genome Database for Rosaceae (GDR)B. The Peach Physical MapC. EST Functional Genomics Database Development

V. FUTURE PROSPECTSLITERATURE CITED

I. INTRODUCTION

The Rosaceae is a large and diverse family that includes deciduous andevergreen trees, shrubs, and herbs. It consists of about 100 genera andmore than 2,000 species distributed worldwide, although it is mostabundant in the colder and temperate Northern regions. The familyincludes numerous economically important crops, grown for their fruits,nuts, and timber or for their ornamental value. The characteristic flow-ers of this family have radial symmetry and usually have five sepals, fivepetals, and numerous stamens. The number of carpels and the ovaryposition varies, giving rise to different fruit types (achenes, drupes,pomes, or follicles), which are important for sub-family classification.Flowers are usually insect-pollinated and frequently large and showy:a high percentage of all species are actual or potential garden ornamen-tals. Most species have a gametophytic self-incompatibility system thatprevents selfing and requires the presence of two inter-compatible geno-types for fruit production. The family is divided into four subfamilies:Spiraeoideae, Maloideae, Prunoideae, and Rosoideae (Rehder 1947).The three latter subfamilies encompass major cultivated species and willbe described in more detail.

The ability of biochemical and DNA-based markers to identify homol-ogous loci in different species is one of their most important properties.Comparing the positions of homologous markers in the linkage maps ofdifferent species allows the degree of resemblance between theirgenomes to be established. Synteny, initially defined as the occurrenceof two or more genes on the same chromosome, but more recentlyexpanded to describe the similarity between the chromosomes of twospecies, was studied in the early days of marker discovery, whenisozymes were almost the only kind of markers available for these stud-ies (Tanksley 1983). With the development of DNA markers, such asrestriction fragment length polymorphisms (RFLPs), maps covering thewhole genome could be produced relatively quickly, and the use of thesame DNA probes in mapping populations of different species yieldedcomparable maps. Tanksley et al. (1992) analyzed the tomato and potatogenomes, and found that the two genomes have an essentially identicalconstitution, with the exception of five paracentric inversions. The com-

176 P. ARÚS, T. YAMAMOTO, E. DIRLEWANGER, AND A. ABBOTT

04_4453.qxd 10/20/05 3:06 PM Page 176

parison of rice with maize, which are more distant, was undertaken byAhn and Tanksley (1993). In spite of the differences in genome size(about 6 times larger in maize) and chromosome number (x = 10 inmaize and x = 12 in rice), important syntenic regions between these twospecies were identified, accounting for 62% of the maize and 70% of therice linkage maps. Later results established that in general there is a highlevel of genetic conservation between members of the same family, asdemonstrated in the Poaceae (Devos and Gale 2000), Solanaceae (Dogan-lar et al. 2003), Brassicaceae (Lukens et al. 2003), and Fabaceae (Choi etal. 2004), but synteny decreases considerably between species of differ-ent families (Dominguez et al. 2003).

Information on comparative mapping in the Rosaceae has been verylimited, until recently. The use of markers and map construction startedlater in this family than in others, and the first saturated maps with trans-ferable markers were produced in the late 1990s (Joobeur et al. 1998;Maliepaard et al. 1998), resulting in a delay with respect to other herba-ceous crops, more easily amenable to genetic studies than fruit trees thatare woody perennials and have a long intergeneration period. The devel-opment of simple-sequence repeat (SSR), or microsatellite markers, hasbeen widespread in the Rosaceae crops (Cipriani et al. 1999; Liebhardtet al. 2002; Sargent et al. 2004; Graham et al. 2004) in the last five years.In addition to their good properties as markers, such as codominance,polymorphism, abundance, and suitability for automation (Weber andMay 1989), SSRs have a good rate of transferability among closely relatedRosaceae species (Dirlewanger et al. 2002), and occasionally among gen-era within the same subfamily (Yamamoto et al. 2001b), and have beenused for synteny studies. Comparisons between species of different sub-families require more transferable markers, such as RFLPs, which havebeen used to a more limited extent for map construction in species ofthis family. Our objective in this review is to summarize the recentprogress in this area, discuss the importance and application of theresults in plant breeding, and identify where additional research isneeded to completely elucidate the genome relationships of this eco-nomically important plant family.

II. GENETIC MAPS IN THE MAIN ROSACEAE SPECIES

A. Subfamily Prunoideae

The five genera in the subfamily Prunoideae are woody plants, eithertrees or shrubs. The crop species of this subfamily belong to its largestgenus, Prunus, and produce drupes as fruits, commonly called “stonefruits.” The most important species of this genus belong to the three

4. SYNTENY IN THE ROSACEAE 177

04_4453.qxd 10/20/05 3:06 PM Page 177

subgenera, Amygdalus, Prunophora, and Cerasus, in which it is divided,including peach (Prunus persica L. Batsch), almond (Prunus dulcisMill.), apricot (Prunus armeniaca L.), European plum (Prunus domes-tica L.), Japanese plum (Prunus salicina Lindl.), sweet cherry (Prunusavium L.), and sour cherry (Prunus cerasus L.). Several other species,such as myrobalan plum (Prunus cerasifera Ehrh.) or Sainte Lucie cherry(Prunus mahaleb L.), are used mainly as Prunus rootstocks. Productionof all stone fruits equals 32 million tonnes (FAOSTAT data, 2003,http://faostat.fao.org), ranking second in importance of all temperatefruits, after apple. The base chromosome number of Prunus is x = 8, withmost of the cultivated species being diploids, with the exception of sourcherry (2n = 4x = 32) and the European plum (2n = 6x = 48).

Peach, the most economically important species of the genus Prunus,has distinct advantages that make it more suitable than others for geneticand genomic analysis. Peach has a short juvenile phase (2 to 3 years)compared to most other fruit tree species, and a small haploid genomeof approximately 290 Mbp (Baird et al. 1994), only about twice the sizeof the Arabidopsis thaliana genome (Arumuganathan and Earle 1991).Moreover, peach is genetically the best characterized Prunus species,with many Mendelian genes controlling morphological traits (Hesse1975; Scorza and Sherman 1996; Monet et al. 1996), and well developedgenomic tools that will be detailed in this review. These attributes makepeach a good model species for the Rosaceae (Abbott et al. 2002).

1. Subgenus Amygdalus. The most important crops of this subgenus arepeach and almond. They can be intercrossed and produce fertile hybridsbut have gross differences in other respects: peach is a self-compatiblespecies with a low level of variability and is used for its fruit, whereasalmond is a highly polymorphic and self-incompatible species used forits seed. The first published map in Prunus (Chaparro et al. 1994) wasconstructed with 83 RAPDs, one isozyme gene, and four morphologicalsingle-gene characters in 96 F2 progeny, obtained from the cross betweentwo peach lines, NC174RL and ‘Pillar’. This map covered a total distanceof 396 cM and identified 15 of the 16 linkage groups expected. Mostmarkers were dominant and linkage could be detected only for markersin coupling phase.

Interspecific F2 or backcross populations between peach and otherspecies have also been used successfully, due to their high degree of seg-regation, compared to the low variability found in peach intraspecificpopulations. Foolad et al. (1995) were the first to publish one such map,using an almond × peach F2 population. The first map of almond wasconstructed entirely with codominant markers (RFLPs and isozymes)


04_4453.qxd 10/20/05 3:06 PM Page 178

using the F1 progeny between ‘Ferragnès’ and ‘Tuono’ (Viruel et al.1995). In total, 16 maps, constructed with 14 populations involvingonly species of the Amygdalus subgenus (peach, almond, P. ferganen-sis, and P. davidiana), have been published to date and their character-istics are summarized in Table 4.1.

Six of these maps, and 10 more in other Prunus subgenera, have beenobtained from crosses between two partially heterozygous and generallyunrelated trees. These full-sib populations, also termed F1 segregatingprogenies, are the common type of breeding populations for many fruittree species, which explains their abundance and interest. Given the gen-erally self-incompatible nature of some species, such as almond, cherry,plum, or apple, this is often the only possible kind of population. Mapconstruction in these progenies with predominantly dominant markersis usually done with the pseudo-testcross or two-way pseudo-testcrossmethod (Hemmat et al. 1994; Grattapaglia and Sederoff 1994) thatimplies the construction of two maps, one for each parent of the cross.Each map contains all the markers heterozygous in each parent. Whenusing codominant markers (RFLPs or SSRs), the majority of them seg-regate as a backcross (Viruel et al. 1995), but a certain number of mark-ers are heterozygous in both parents, giving rise to 1:2:1 or 1:1:1:1segregation ratios. These latter markers can be mapped in both parentsand thus be used as anchors to establish the connection between the twoparental maps. As peach is self-compatible, F2 populations can beobtained, allowing a simpler and more standard mapping procedure.

The map constructed with the F2 of the cross between ‘Texas’ almondand ‘Earlygold’ peach has been adopted by the stone fruit community asthe reference for the genus. This map, originally constructed by a con-sortium of European groups (Joobeur et al. 1998), was obtained only withcodominant markers (235 RFLPs and 11 isozymes). The ‘Texas’ × ‘Early-gold’ map (abbreviated T×E) was considered to be saturated, as all mark-ers could be placed on the expected eight linkage groups (G1 to G8),average marker density was high (2.0 cM/marker), and gaps were scarceand small (only two gaps >10 cM, the largest 12 cM). New high-qualitymarkers were added later to T×E (Aranzana et al. 2003, Dirlewanger et al.2004a) to produce the current map with 562 markers (361 RFLPs, 185SSRs, 11 isozymes, and 5 STSs), covering a total distance of 519 cM, withhigh density (<1 cM/marker) and largest gap of 7 cM. This map has beena useful resource for the Prunus community: markers from it have beenused for the construction of other Prunus maps, allowing map compari-son and construction of framework maps (maps with a low number ofselected markers covering most of the genome) in other populations andspecies; a common terminology for linkage group numbers has been


04_4453.qxd 10/20/05 3:06 PM Page 179

180

Tab

le 4

.1.

Pru

nu

sli

nka

ge m

aps

con

stru

cted

on

ly w

ith

sp

ecie

s of

th

e A

myg

dal

us

subg

enu

s.

No.

Tot

alL

onge

st%

No.

Mos

t co

mm

on

lin

kage

dis

tan

cega

pu

nli

nke

dP

opu

lati

onz

Typ

eS

pec

ies

mar

kers

ym

arke

r ty

pes

xgr

oup

s(c

M)w

(cM

)lo

civ

Ref

eren

ces

NC

174R

L ×

Pil

lar

F2

Pea

ch88

RA

PD

(94

),

1539

623

8C

hap

arro

et

al.

(96)

mor

phol

ogic

al

(199

4)(5

)

New

Jer

sey

Pil

lar

F2

Pea

ch47

RF

LP

(71

),

833

234

28R

ajap

akse

et

al.

× K

V 7

7119

(71

)R

AP

D (

18)

(199

5)

Lov

ell

×N

emar

edF

2P

each

153

AF

LP

(98

),

1512

9742

12L

u e

t al

. (19

98)

(96)

SS

R (

1)

Fer

jalo

u J

alou

sia(r

)F

2P

each

124

SS

R (

53),

7

518

260

Eti

enn

e et

al.

(20

02);

×

Fan

tasi

a (6

3)R

FL

P (

40)

Dir

lew

ange

r et

al. (

un

p.)

Aka

me

×Ju

seit

ou

F2

Pea

ch17

8S

SR

(53

),

7u57

115

0Y

amam

oto

et a

l.

(126

)A

FL

P (

19)

(200

1a);

T.

Yam

amot

o (u

np

.)

Fer

ragn

ès ×

Tu

ono

F1

Alm

ond

12

6 R

FL

P (

69),

8

415

170

Joob

eur

et a

l. (

2000

)(6

0)(F

erra

gnès

)(1

74)

RA

PD

(24

)

Alm

ond

99

841

628

0(T

uon

o)

Fel

isia

×B

erti

na

F1

Alm

ond

45

R

FL

P (

92),

8

386

290

Bal

lest

er e

t al

. (1

34)

(Fel

isia

)(6

5)R

AP

D (

8)(2

001)

Alm

ond

39

734

928

5(B

erti

na)

04_4453.qxd 10/20/05 3:06 PM Page 180

Gar

fi ×

Nem

ared

F

2A

lmon

d ×

51R

FL

P (

90),

7u

474

320

Jáu

regu

i et

al.

(20

01)

(113

)p

each

isoz

yme

(10)

Pad

re ×

54P

455

F2

Alm

ond

×16

1R

FL

P (

89),

8

1144

360

Foo

lad

et

al. (

1995

);

(64)

pea

chis

ozym

e (5

)B

liss

et

al. (

2002

)

Tex

as ×

Ear

lygo

ld

F2

Alm

ond

×56

2R

FL

P (

66),

8

519

70

Joob

eur

et a

l. (

1998

);

(82)

pea

chS

SR

(33

)D

irle

wan

ger

et a

l.

(200

4a)

P. c

eras

ifer

a×

F1

Alm

ond

×16

6S

SR

(99

),

871

620

0D

irle

wan

ger

Fel

inem

(10

1)p

each

S

TS

(1)

et a

l. (

2004

b)(F

elin

em)

Su

mm

ergr

and

×P

.F

1P

. dav

idia

na

133

RF

LP

(42

),

946

522

0F

oulo

ngn

e et

al.

d

avid

ian

a(7

7)p

aren

tR

AP

D (

32)

(200

3)

Su

mm

ergr

and

×P

. F

2P

each

×P

.15

3R

FL

P (

43),

8

874

180

Fou

lon

gne

et a

l.

dav

idia

na

(99)

dav

idia

na

AF

LP

(40

)(2

003)

IF73

1082

8 ×

P.

BC

1(P

each

×P

. 10

9R

FL

P (

68),

10

521j

294

Det

tori

et

al.

ferg

anen

sis

ferg

anen

sis)

S

SR

(16

)(2

001)

(70)

×p

each

z Pop

ula

tion

siz

e is

in

par

enth

esis

.y N

um

ber

of m

app

ed m

arke

rs. F

or F

1p

roge

nie

s, i

n p

aren

thes

is a

fter

th

e fe

mal

e p

aren

t n

um

ber

of m

arke

rs, t

otal

nu

mbe

r of

mar

kers

loc

ated

on

th

em

ap.

x In

par

enth

esis

, per

cen

tage

of

the

two

mos

t co

mm

on k

ind

s of

mol

ecu

lar

mar

kers

use

d f

or m

app

ing.

For

F1

pro

gen

ies

this

per

cen

tage

ref

ers

to t

he

tota

l n

um

ber

of m

arke

rs u

sed

.wj =

map

s co

nst

ruct

ed w

ith

Join

Map

(van

Ooi

jen

an

d V

oorr

ips,

200

2) s

oftw

are;

the

rest

wer

e co

nst

ruct

ed w

ith

Map

Mak

er (L

and

er e

t al.

198

7). D

is-

tan

ces

are

Kos

ambi

.v P

rop

orti

on o

f m

arke

rs a

ssay

ed n

ot f

alli

ng

wit

hin

an

y of

th

e li

nka

ge g

rou

ps.

uP

opu

lati

ons

segr

egat

ing

for

the

G6-

G8

reci

pro

cal t

ran

sloc

atio

n. T

he

con

figu

rati

on o

f T×E

has

bee

n ta

ken

for

the

calc

ula

tion

of t

he

nu

mbe

r of

mar

k-er

s in

th

e m

ap a

nd

tot

al d

ista

nce

.

181

04_4453.qxd 10/20/05 3:06 PM Page 181

established; its high polymorphism allows mapping of markers that aremonomorphic in other populations (particularly from peach); markersfrom this map can be used to saturate specific regions of interest in othermaps and, finally, RFLPs chosen from this map have been used as start-ing points for the construction of the Prunus physical map (http://www.genome.clemson.edu/gdr/). Given that the number of generallywell-distributed SSRs is high (185), this map also provides a publiclyavailable source of mapped, highly polymorphic markers that can bedetected with relatively simple and cheap methods, and are more suitableto breeding applications than other high-quality markers such as RFLPs.

Most of these maps were constructed with codominant markers, witha progressive shift from RFLPs to SSRs in the most recent maps. Themaps range in size from 332 to 1,297 cM, although for the majority ofthose with a reasonable number of markers (>150) this range is approx-imately 500–800 cM. The total distance of most of the maps was smallerthan that commonly found in other species, of approximately 100 cM perchromosome, which may be explained in part by the small size of thePrunus genome. The relationship between chromosomes and linkagegroups has not been established yet, but linkage group 1 (G1) of Prunusis longer and more populated with markers than the other linkage groupsin most maps (i.e., 121 markers and a distance of 87 cM of G1 vs. an aver-age of 63 markers per linkage group and a distance of 61 cM for the restof the linkage groups in T×E), and one of the chromosomes of Prunus isclearly longer than the rest (Salesses and Mouras 1977; Corredor et al.2004), suggesting that G1 corresponds to chromosome 1.

2. Subgenus Prunophora. Linkage map construction started eight yearslater in this subgenus, which includes apricot and plum, than in Amyg-dalus. The first published map was in apricot and used mainly AFLPs(Hurtado et al. 2002). A detailed map, constructed in part with markersselected from T×E, was later produced with the F1 population of thecross between ‘Polonais’ and ‘Stark Early Orange’, and is the basis forthe comparison between the species of these two subgenera. The uniquemap involving a plum species was obtained by Dirlewanger et al. (2004b)in one of the parents of a three-way cross between myrobalan plum andthe almond × peach rootstock ‘Felinem’. This map was constructedmainly with SSRs, most common to the T×E population.

The characteristics of the 6 maps obtained with 4 populations ofcrosses between species of this subgenus are summarized in Table 4.2.They are similar to those of the Amygdalus subgenus, with distancesranging from 467 to 699 cM. The number of linkage groups is reasonablyclose to the expected eight in the maps using codominant markers.


04_4453.qxd 10/20/05 3:06 PM Page 182

3. Subgenus Cerasus. Six maps have been published in species of thissubgenus using five populations (Table 4.2). The earliest was con-structed in sweet cherry with RAPDs (Stockinger et al. 1996). Anothermap created exclusively with isozyme genes was obtained using datafrom two interspecific cherry progenies (Boskovic and Tobutt 1998).This map includes a total of 47 segregating isozyme genes, from which34 were aligned into seven linkage groups. Sour cherry, an importantcrop in this subgenus, is tetraploid. Isozyme analysis detected a clearallopolyploid behaviour (Beaver and Iezzoni 1993) and the map obtainedby Wang et al. (1998), with RFLPs in an F1 progeny of this species, con-firmed these findings, although the segregation of a few loci suggestedthat a low degree of intergenomic pairing and recombination may occur(Wang et al. 1998). Map sizes in Cerasus are consistent with thoseobtained in species of the other subgenera, but given that the total num-ber of markers is generally lower, the number of linkage groups is dif-ferent than that expected, and the size of the largest gaps and theproportion of unlinked markers are higher than in other more populatedmaps.

B. Subfamily Maloideae

This subfamily, characterized by a distinctive pome fruit, includesapproximately 1,000 species in 30 genera (Westwood 1978), some ofwhich are important fruit tree species, such as apple (Malus spp.), pear(Pyrus spp.), quince (Cydonia oblonga Mill.), loquat (Eryobotrya japon-ica (Thunb.) Mill.), medlar (Mespilus germanica L.), hawthorn (Cratae-gus spp.), and others (Kovanda 1965; Westwood 1978; Luby 2003).About 58 million tonnes of apple fruits are produced worldwide inmore than 90 countries (FAOSTAT data, 2003, http://faostat.fao.org),and account for 12.1% of all fruit production. Seventeen million tonnesof pears are produced (3.6% of world fruit production), and the otherfruit species belonging to Maloideae account for less than 1%.

The basic chromosome number is x = 17 for all Maloideae genera (Sax1931, 1932; Kovanda 1965). While triploid and tetraploid plants havebeen found in Malus and Pyrus, only diploids are known in Eryobotryaand Cydonia (Sax 1932; Kovanda 1965). The genome size of genera inMaloideae ranges from 450 to 800 Mbp/haploid genome, which is 2 to3 times larger than species in the other subfamilies, consistent withtheir polyploid origin (Dickson et al. 1992).

1. Apple. The genetic linkage maps of apple are listed in Table 4.3.Apple has a long juvenile period and is self-incompatible, and genetic


04_4453.qxd 10/20/05 3:06 PM Page 183

184

Tab

le 4

.2.

Pru

nu

sli

nka

ge m

aps

of t

he

Pru

nop

hor

aan

d C

eras

us

subg

ener

a.

Mos

tco

mm

on

No.

Tot

alL

onge

st%

No.

mar

ker

lin

kage

dis

tan

cega

pu

nli

nke

dP

opu

lati

onz

Typ

eS

pec

ies

mar

kers

yty

pes

xgr

oup

s(c

M)w

(cM

)lo

civ

Ref

eren

ces

Pru

nop

hor

aP

. cer

asif

era

×F

1P

. cer

asif

era

93S

SR

(98

),

852

524

1D

irle

wan

ger

et a

l.

Fel

inem

(10

1)S

CA

R (

2)(2

004b

)P

olon

ais

×S

tark

F

1A

pri

cot

110

(212

)R

FL

P (

45),

8

538

330

Lam

bert

et

al.

Ear

ly O

ran

ge

(Pol

onai

s)A

FL

P (

31)

(200

4)(S

EO

) (1

42)

Ap

rico

t (S

EO

)14

1R

FL

P (

40),

8

699

310

AF

LP

(38

)G

old

rich

×F

1A

pri

cot

132

(176

)A

FL

P (

62),

8

511j

2422

Hu

rtad

o et

al.

V

alen

cian

o (G

old

rich

)R

AP

D (

25)

(200

2)(8

1)A

pri

cot

80A

FL

P (

60),

7

467j

2835

(Val

enci

ano)

RA

PD

(24

)S

EO

×T

yrin

thos

F

2A

pri

cot

211

AF

LP

(85

),

1160

2j29

20V

ilan

ova

et a

l.(7

6)S

SR

(14

)(2

003)

Cer

asu

sN

apol

eon

×F

1S

wee

t ch

erry

, 34

Isoz

ymes

7

174r

u24

ru28

Bos

kovi

c an

d

P. i

nci

sa(6

3)P

. in

cisa

and

(100

)T

obu

tt (

1998

)an

d N

apol

eon

P

. nip

pon

ica

×P

. nip

pon

ica

(47)

Em

per

or

Mic

ro-

Sw

eet

cher

ry89

RA

PD

(98

),

1050

327

3S

tock

inge

r et

al.

F

ran

cis

(56)

spor

e-is

ozym

e (1

996)

der

ived

(2

)ca

lli

04_4453.qxd 10/20/05 3:06 PM Page 184

Rh

ein

isch

e F

1S

our

cher

ry

126

(126

)R

FL

P (

100)

1946

2j21

12W

ang

et a

l. (1

998)

Sch

atte

nm

orel

le

(RS

)(R

S)

×E

rdi

Sou

r ch

erry

95

1627

9j21

19B

oter

mo

(EB

) (E

B)

(86)

Rég

ina

×L

apin

s F

1S

wee

t ch

erry

68

(99

)S

SR

s (1

00)

1163

926

1D

irle

wan

ger

et a

l.(1

33)

(Rég

ina)

(200

4a)

Sw

eet

cher

ry

549

495

3010

(Lap

ins)

z Pop

ula

tion

siz

e is

in

par

enth

esis

.y N

um

ber

of m

app

ed m

arke

rs. F

or F

1p

roge

nie

s, i

n p

aren

thes

is a

fter

th

e fe

mal

e p

aren

t n

um

ber

of m

arke

rs, t

otal

nu

mbe

r of

mar

kers

loc

ated

on

th

em

ap.

x In

par

enth

esis

, per

cen

tage

of

the

two

mos

t co

mm

on k

ind

s of

mol

ecu

lar

mar

kers

use

d f

or m

app

ing.

For

F1

pro

gen

ies

this

per

cen

tage

ref

ers

to t

he

tota

l n

um

ber

of m

arke

rs u

sed

.wj

= m

aps

con

stru

cted

wit

h J

oin

Map

(va

n O

oije

n a

nd

Voo

rrip

s, 2

002)

sof

twar

e; r

u =

map

s co

nst

ruct

ed w

ith

LIN

KE

M (

Vow

den

et

al.

1995

) an

dli

nka

ge m

easu

red

in

rec

ombi

nat

ion

un

its;

th

e re

st w

ere

con

stru

cted

wit

h M

apM

aker

(L

and

er e

t al

. 198

7). D

ista

nce

s ar

e K

osam

bi.

v Pro

por

tion

of

mar

kers

ass

ayed

not

fal

lin

g w

ith

in a

ny

of t

he

lin

kage

gro

up

s.

185

04_4453.qxd 10/20/05 3:06 PM Page 185

186

Tab

le 4

.3.

Lin

kage

map

s of

ap

ple

an

d p

ear.

No.

Tot

al%

Cu

ltiv

ar

No.

Mos

t co

mm

on

lin

kage

dis

tan

ceL

onge

stu

nli

nke

dP

opu

lati

onz

nam

em

arke

rsy

mar

ker

typ

esx

grou

ps

(cM

)wga

p (

cM)

loci

vR

efer

ence

s

Ap

ple

Rom

e B

eau

ty ×

Rom

e 15

6 (4

27)

RA

PD

s, I

sozy

mes

,21

~68

2~

208

Hem

mat

et

al. (

1994

)W

hit

e A

nge

l (5

6)B

eau

tyR

FL

Ps

Wh

ite

253

RA

PD

s, I

sozy

mes

, A

nge

lR

FL

Ps

2495

0~

282

Wij

cik

McI

nto

sh

Wij

cik

238

RA

PD

s, I

sozy

mes

211,

206j

2711

Con

ner

et

al. (

1997

)(W

M)

×N

Y

McI

nto

sh75

441-

67 (

114)

,

WM

×N

Y 7

5441

-58

NY

754

41-6

711

0R

AP

Ds,

Iso

zym

es21

692j

2414

Con

ner

et

al. (

1997

)(1

72)

NY

754

41-5

818

3R

AP

Ds,

Iso

zym

es20

898j

234

Idu

na

×A

679-

2 (9

5)Id

un

a65

RA

PD

s (1

00)

938

6j22

23S

egli

as a

nd

Ges

sler

A

679-

213

5R

AP

Ds

(100

)14

627j

227

(199

7)

Pri

ma

×F

iest

a (1

52)

Pri

ma

194

(290

)R

FL

Ps

(48)

, 17

842j

2413

+M

alie

paa

rd e

t al

. R

AP

Ds

(41)

(199

8)F

iest

a16

3R

FL

Ps

(53)

, 17

984j

33R

AP

Ds

(33)

04_4453.qxd 10/20/05 3:06 PM Page 186

Fie

sta

×D

isco

very

F

iest

a43

9 (8

40)

AF

LP

s (5

0),

171,

144j

262+

Lie

bhar

d e

t al

. (20

03a)

(267

)S

SR

s (2

6)D

isco

very

499

AF

LP

s (5

1),

171,

455j

26S

SR

s (2

2)

Pea

rK

inch

aku

×K

osu

i K

inch

aku

120

RA

PD

s (1

00)

1876

8j27

10Ik

etan

i et

al.

(20

01)

(82)

Kos

ui

78R

AP

Ds

(100

)22

508j

2115

Bar

tlet

t ×

Hou

sui

Hou

sui

180

AF

LP

s (6

1),

(63)

SS

Rs

(36)

2099

5j23

6Y

amam

oto

et a

l.

Bar

tlet

t25

6A

FL

Ps

(70)

, (2

002,

200

4a)

SS

Rs

(30)

191,

020j

243

z Pop

ula

tion

siz

e is

in

par

enth

esis

. All

pop

ula

tion

s ar

e F

1se

greg

atin

g p

roge

nie

s.y N

um

ber

of m

app

ed m

arke

rs. I

n p

aren

thes

is a

fter

th

e fe

mal

e p

aren

t n

um

ber

of m

arke

rs, t

otal

nu

mbe

r of

mar

kers

loc

ated

on

th

e m

ap.

x In

par

enth

esis

, per

cen

tage

of

the

two

mos

t co

mm

on k

ind

s of

mol

ecu

lar

mar

kers

use

d f

or m

app

ing

refe

rred

to

the

tota

l n

um

ber

of m

arke

rs u

sed

.wj =

map

s co

nst

ruct

ed w

ith

Join

Map

(van

Ooi

jen

an

d V

oorr

ips,

200

2) s

oftw

are;

the

rest

wer

e co

nst

ruct

ed w

ith

Map

Mak

er (L

and

er e

t al.

198

7). D

is-

tan

ces

are

Kos

ambi

.v P

rop

orti

on o

f m

arke

rs a

ssay

ed n

ot f

alli

ng

wit

hin

an

y of

th

e li

nka

ge g

rou

ps.

Wh

en “

+”

this

pro

por

tion

was

cal

cula

ted

fro

m t

he

tota

l n

um

ber

ofm

arke

rs u

sed

in

bot

h p

aren

ts.

187

04_4453.qxd 10/20/05 3:06 PM Page 187

analysis typically is performed on the full-sib progeny of a single cross.The first genetic linkage map of apple was created from a ‘Rome Beauty’× ‘White Angel’ F1 population combining RAPDs, isozymes, and RFLPs(Hemmat et al. 1994). The linkage map for ‘White Angel’ consisted of 253markers arranged in 24 linkage groups and extended for 950 cM. Themap of ‘Rome Beauty’ consisted of 156 markers in 21 linkage groups.RAPDs were also the predominant markers in the maps constructed byConner et al. (1997) and Seglias and Gessler (1997).

Two saturated maps have been published in apple. The first, reportedby Maliepaard et al. (1998), was based on the F1 progeny of the crossbetween the cultivars ‘Prima’ and ‘Fiesta’ and was constructed using amajority of transferable markers (RFLPs, isozymes, and SSRs). The mapsof each parent were well aligned with 67 multi-allelic molecular mark-ers, in which 17 linkage groups were found, putatively correspondingto the basic chromosome number. Scab resistance (Vf ) and rosy leaf curl-ing aphid resistance (Sd1) genes were identified at the bottom of link-age group 1 and at the top of linkage group 7, respectively, in thesewell-organized reference maps. The fruit acidity locus, Ma, was locatedat the top of group 16, while the self-incompatibility locus S was foundat the bottom of group 17. The second saturated apple map is based on267 F1 progeny from a cross of ‘Fiesta’ × ‘Discovery’ (Liebhard et al. 2002;Liebhard et al. 2003a). The maps of ‘Fiesta’ and ‘Discovery’, including115 and 112 SSRs, respectively, could be integrated and anchored by ca.100 SSR loci, and were aligned to the maps of Maliepaard et al. (1998).The total distance of these maps ranged from 842 to 1455 cM, approxi-mately twice the distance found in Prunus, as expected considering thetetraploid nature of apple.

SSR markers are currently the best choice for comparing and aligningdifferent genetic linkage maps within a species and they have been usedto align apple maps initially constructed with RAPDs or AFLPs. Hem-mat et al. (2003) established the homology between linkage groups of dif-ferent apple maps of ‘Rome Beauty’, ‘White Angel’, ‘Wijcik McIntosh’,and NY 75441-58 (Hemmat et al. 1994; Conner et al. 1997), by using 41SSR primer sets. Their maps could also be partially aligned to that ofMaliepaard et al. (1998), to which 13 out of 17 linkage groups wereanchored. Ten SSR markers were also mapped by Gianfranceschi et al.(1998) in the population used by Seglias and Gessler (1997). Eight ofthem segregated in both parents, allowing 6 homologous linkage groupsto be identified.

More than 60 major genes in apple have been identified for pest anddisease resistances, and fruit, flower, reproductive, and plant attributes(Brown 1992; Janick et al. 1996; Alston et al. 2000). However, only a


04_4453.qxd 10/20/05 3:06 PM Page 188

small number of these phenotypic characteristics have been identifiedin genetic linkage maps. The use of common SSRs in different popula-tions may help to establish a consensus apple map with which it wouldbe possible to compare the position and function of genes of interestfound in different populations.

2. Pear. The genetic linkage maps of pear are also included in Table 4.3.The first molecular linkage maps were constructed in the Japanese pear(Pyrus pyrifolia Nakai) cultivars ‘Kinchaku’ and ‘Kosui’ using their 82F1 progenies (Iketani et al. 2001). The linkage maps of ‘Kinchaku’ and‘Kosui’ were constructed only with RAPDs and allowed the detection of18 and 22 linkage groups, respectively. It is believed that these 2 mapscover at least half of the total pear genome. The resistance to pear scabdisease (Vn) and susceptibility to black spot disease (A) were identifiedin the genetic map of ‘Kinchaku’. Several RAPD markers had significantlinkage to pear scab resistance and black spot susceptibility.

Genetic linkage maps of the European pear (Pyrus communis L.‘Bartlett’) and the Japanese pear (P. pyrifolia (Burm.) Nakai ‘Housui’) wereconstructed using their interspecific F1 progenies (Yamamoto et al. 2002;Yamamoto et al. 2004a). The map of the seed parent, ‘Bartlett’, consistedof 256 loci, distributed on 19 linkage groups. Out of 76 SSRs mapped, 32,39, and 5 were derived from Pyrus, Malus, and Prunus, respectively. Themap of ‘Housui’ contains 180 loci, including 64 SSRs (29 pear, 29 apple,6 Prunus SSRs) on 20 linkage groups. The two pear maps were alignedusing 37 codominant markers with segregating alleles in both parents.These pear maps may cover more than 80% of the total pear genome.

C. Subfamily Rosoideae

There are three main crops in the Rosoideae subfamily, with a basicchromosome number of x = 7: strawberry, rose, and raspberry. Straw-berry is a species of the genus Fragaria, which includes 12 species withdifferent degrees of ploidy, from the diploid wild strawberry (F. vesca)to the octoploid modern garden strawberry (F. × ananassa), synthesisedin the middle of the 18th century from the cross between two octoploidwild species, F. chiloensis and F. virginiana (Jones 1976). The edible partof strawberries consists of an enlarged, fleshy fruit receptacle that sup-ports the tiny true fruits (achenes). Diploid strawberry species have thesmallest genomes within the cultivated Rosaceae, with 164 Mbp in theF. vesca genome (Akiyama et al. 2001).

In spite of its economic importance, the cultivated strawberry is poorlycharacterised genetically. This is in part because of its complex genetic


04_4453.qxd 10/20/05 3:06 PM Page 189

background. It is an octoploid species with 2n = 56, with an unknowngenomic composition. Only one map has been published (Lecerteau-Köhler et al. 2003) based on an F1 progeny between two octoploid lines.This map was made with a large number of AFLPs (789) that coalescedinto 58 linkage groups. Based on the presence of linkage groups com-posed only of single-dose restriction fragments (SDRF) in coupling, andthe frequency of multiplex vs. simplex markers (Wu et al. 1992; Da Silvaet al. 1993), the authors concluded that the octoploid strawberry has amixed diploid/polyploid behavior and that at least two of the compo-nent genomes are duplicated. One way of simplifying the complexity of the strawberry genome would be to develop detailed maps in diploidrelatives and use these maps as references for polyploid map construc-tion, as has been done in other polyploid crops, including alfalfa (Diwanet al. 2000) and potato (Milbourne et al. 1998). Two maps have been con-structed so far in the diploid wild strawberry, F. vesca, which seems theideal organism for this purpose. The first one was with an F2 progeny ofthe cross between two F. vesca accessions by Davis and Yu (1997) usingRAPDs (75), isozymes (3), and morphological characters (2). All thesemarkers mapped to the expected 7 linkage groups covering a total dis-tance of 445 cM. From the nature of most of the markers used (RAPDs),it is unlikely that this map can be used for genome comparisons in Fra-garia. A more adequate map for this purpose is the one constructedwith 78 markers [68 SSRs, 6 gene-specific markers, one sequence char-acterized amplified region (SCAR), and three morphological characters]by Sargent et al. (2004), using an interspecific F2 population (F. vesca ×F. nubicola). Seventy-six of these markers could be placed on seven link-age groups spanning a distance of 448 cM. Given its high level of poly-morphism and the work already done on mapping, this population maybecome the reference for strawberry in the future.

Rose (Rosa spp.) cultivars are a complex of different hybrids betweenvarious diploid and tetraploid species with different ploidy levels—diploid, triploid, and tetraploid. The rose achenes are surrounded by thehypanthium (formed by the bottom of the petals, sepals, and stamensstuck together), giving a more or less fleshy, fruit-like structure, calledthe hip. Rose maps have been elaborated in three populations with theobjective of establishing the location of major genes or QTLs responsi-ble for the inheritance of some of the most important characters of flowerquality and disease resistance. These maps were constructed almostentirely with dominant markers (RAPDs and AFLPs), which impliesthat they cannot be compared or used for synteny analysis with othermembers of the Rosaceae. Two of these maps were obtained in diploidF1 populations (Debener and Mattiesch 1999; Crespel et al. 2002) andone in an F2 between two tetraploid genotypes (Rajapakse et al. 2001).


04_4453.qxd 10/20/05 3:06 PM Page 190

Map sizes were generally small, as in other Rosaceae species, rangingfrom 238 to 370 cM in the diploid genotypes, to 628 to 902 for thetetraploids.

The raspberry belongs to the genus Rubus, which also includes otherberries, such as dewberries, brambles, and blackberries. The flowers ofRubus are structurally rather similar to those of strawberries; however,in Rubus each carpel develops into a small drupe (drupelet), with themesocarp becoming fleshy and the endocarp hardening and forming atiny pit that encloses a single seed. Since there are many carpels perflower, there are many drupelets, and the “fruit” of a blackberry or rasp-berry is really an aggregate of drupelets. Raspberries are diploid, with agenome of similar size to Prunus (294 Mbp) (Arumuganatan and Earle1991), but blackberries have different levels of ploidy, from tetraploidto octoploid. A map with 273 markers, including 34 SSRs, was con-structed by Graham et al. (2004) in a diploid red raspberry (Rubusidaeus) F1 population. The map included 9 linkage groups, two morethan the seven expected, covering a distance of 789 cM. Several QTLsfor spiny phenotype and root sucker production were placed on thismap, the first produced in Rubus.

III. MAP COMPARISONS

A. Within the Prunus Genus

Common markers mapped in the reference T×E Prunus and in otherPrunus populations have been used to compare their map positions indifferent species and interspecific hybrids. Table 4.4 summarizes theseresults for the 11 populations (corresponding to 16 maps) having morethan 25 markers in common with T×E. These maps allow comparisonsbetween seven species: peach, almond, apricot, sweet cherry, myrobalanplum, P. ferganensis, and P. davidiana. The part of the genome of T×Ecovered with these comparisons is on average 57%, with a range of21–78%.

Markers used for synteny analysis are of three kinds: RFLPs andisozymes, both known to be highly transferable across genus and fami-lies, and more recently, SSRs. The excellent properties of SSRs and thedevelopment of hundreds since the first set reported by Cipriani et al.(1999) have made SSRs the markers of choice for many uses in Prunusgenetics and breeding. Although systematic studies on SSR transfer-ability among Prunus species have not been made, when SSRs devel-oped in one species have been used in another, they often have beenuseful (i.e., give amplified polymorphic DNA fragments of about the


04_4453.qxd 10/20/05 3:06 PM Page 191

192

Tab

le 4

.4.

Com

par

ison

of

Pru

nu

sli

nka

ge m

aps

wit

h t

he

refe

ren

ce ‘T

exas

’ ×‘E

arly

gold

’ (T

×E)

map

.

Pai

red

t

test

An

chor

s%

Sam

eN

on-

% o

f %

of

com

par

ison

w

ith

grou

p a

sco

lin

ear

T×E

com

mon

wit

hP

opu

lati

onM

ap t

ypez

T×E

yT

×Ex

mar

kers

wd

ista

nce

vd

ista

nce

uT

×Et

Ref

eren

ces

Tex

as ×

Ear

lygo

ldF

256

210

00

100

100

—D

irle

wan

ger

et a

l. (

2004

a)

Gar

fi ×

Nem

ared

(8)

F2

5110

00

7811

73.

57**

Jáu

regu

i et

al.

(20

01)

Su

mm

ergr

and

×P

. F

1(P

. dav

idia

na)

5296

264

113

0.98

Fou

lon

gne

et a

l. (

2003

)d

avid

ian

a

Su

mm

ergr

and

×P

. F

257

100

070

196

4.62

**F

oulo

ngn

e et

al.

(20

03)

dav

idia

na

IF73

1082

8 ×

P.

BC

132

100

141

121

1.54

Det

tori

et

al. (

2001

)fe

rgan

ensi

s

P. c

eras

ifer

a×

F1

(P. c

eras

ifer

a)43

933

5319

06.

32**

Dir

lew

ange

r et

al.

(20

04b)

Fel

inem

F1

(Fel

inem

s )87

982

6616

35.

47**

Dir

lew

ange

r et

al.

(20

04b)

Fer

ragn

ès ×

Tu

ono

F1

(Fer

ragn

ès)

53 (

72)

100

364

100

0.01

Joob

eur

et a

l. (

2000

)

F1

(Tu

ono)

4110

01

4811

10.

76

Fel

isia

×B

erti

na

F1

(Fel

isia

)32

(43

)10

00

5711

10.

80B

alle

ster

et

al. (

2001

)

F1

(Ber

tin

a)28

100

257

112

1.23

04_4453.qxd 10/20/05 3:06 PM Page 192

Pol

onai

s ×

Sta

rk E

arly

F

1(P

olon

ais)

49 (

81)

932

6311

52.

19L

ambe

rt e

t al

. (20

04)

Ora

nge

(S

EO

)

F1

(SE

O)

6195

479

152

3.59

**L

ambe

rt e

t al

. (20

04)

Fer

jalo

u J

alou

siaR

×F

249

952

5714

24.

21**

Eti

enn

e et

al.

(20

02)

Fan

tasi

a

Aka

me

×Ju

seit

ous

F2

4598

252

109

0.79

Yam

amot

o et

al.

(u

np

)

Rég

ina

×L

apin

sF

1(R

égin

a)30

971

3423

33.

34**

Dir

lew

ange

r et

al.

(20

04a)

F1

(Lap

ins)

2896

121

323

3.19

**

z In

par

enth

esis

, nam

e of

th

e p

aren

t m

ap f

or F

1se

greg

atin

g p

opu

lati

ons.

y On

ly m

aps

wit

h m

ore

than

25

anch

or p

oin

ts w

ith

T×E

hav

e be

en c

onsi

der

ed. F

or F

1p

roge

nie

s, in

par

enth

esis

aft

er th

e fe

mal

e p

aren

t mar

ker

nu

m-

ber,

tot

al n

um

ber

of m

arke

rs s

tud

ied

in

th

e cr

oss.

x Per

cen

tage

of

anch

or m

arke

rs l

ocat

ed o

n t

he

sam

e li

nka

ge g

rou

p a

s T

×E.

wN

um

ber

of m

arke

rs p

lace

d o

n th

e sa

me

lin

kage

gro

up

as

that

of T

×E b

ut i

n d

iffe

ren

t ord

er (g

ener

ally

pai

rs o

f mar

kers

in in

vert

ed o

rder

; on

ly o

ne

of t

he

two

mar

kers

is

con

sid

ered

).v P

erce

nta

ge o

f th

e T

×E m

ap c

over

ed b

y th

e ot

her

map

: dis

tan

ce o

f T

×E c

over

ed*1

00/t

otal

T×E

dis

tan

ce.

uR

elat

ive

size

of

the

com

mon

map

s: c

omm

on d

ista

nce

cov

ered

in

a m

ap*1

00/c

omm

on d

ista

nce

cov

ered

in

T×E

.t P

aire

d t

-tes

t of

th

e co

mp

aris

on b

etw

een

th

e d

ista

nce

s of

th

e tw

o m

ost

sep

arat

ed c

omm

on m

arke

rs o

f ea

ch l

inka

ge g

rou

p. *

* P

≤0.0

1.s F

or t

he

pop

ula

tion

s se

greg

atin

g fo

r th

e G

6-G

8 re

cip

roca

l tr

ansl

ocat

ion

, th

e T

×E c

onfi

gura

tion

has

bee

n t

aken

for

map

com

par

ison

s.

193

04_4453.qxd 10/20/05 3:06 PM Page 193

expected size). This has occurred generally with peach SSRs used inother species, because peach SSRs were developed first and there aremore available than in any other Prunus species. For example, 55% and45% of the peach SSRs used for variability analysis in apricot (Hormaza2002) or cherry (Dirlewanger et al. 2002), respectively, amplified andwere polymorphic in a sample of cultivars of these species.

The distribution of markers to different linkage groups and their orderwithin each linkage group in all Prunus species comparisons results ina general pattern of complete synteny between all species, suggesting thatthe Prunus genome can be treated as a single genetic entity. This resultis in agreement with the affinity between different species, which can becrossed within the same subgenus, in some cases between subgenera(Amygdalus and Prunophora), and that these crosses occasionally pro-duce fertile offspring (Scorza and Sherman 1996). Some of the figures ofTable 4.4 clearly show this trend, with a percentage of markers locatedin the same group as T×E, generally of 100 or very close to 100, and a verysmall number of non-colinear markers among those that are in the samelinkage group. Given that RFLP probes frequently detect more than one locus in Prunus (Viruel et al. 1995; Joobeur et al. 1998), it is reason-able to think that most of the markers of one map that are not located inthe expected linkage group of T×E correspond to copies of this RFLP thatwere not mapped (probably because they were not segregating) in T×E(Lambert et al. 2004). Moreover, the markers that have a changed orderwithin a linkage group are frequently contiguous and separated by onlya few cM, suggesting that these discrepancies are more likely due to sam-pling errors, leading to slight differences in locus order, than to actualchromosomal rearrangements between the two compared genomes.

The genetic distances between maps were compared with a paired t-test (two-tailed) of the difference between the map distances of the twomost separate anchor markers of each linkage group of T×E, and that ofthe map compared with it. All maps were constructed with MapmakerEXP/3.0 (Lander et al. 1987) software with the exception of that of Det-tori et al. (2001), where JoinMap (van Ooijen and Voorrips 2002) wasused instead. JoinMap usually produces shorter maps than those ofMapMaker (Liebhard et al. 2003a). This may be due to differences in thecalculation of linkage when using the Kosambi mapping function (Stam1993), which was employed in all maps listed in Table 4.4. Thus, wecannot discard that the paired t-test between T×E and the peach × P. fer-ganensis BC1 map of Dettori et al. (2001) would have been significantshould a Mapmaker version of this map be used.

An interesting observation is that some maps are significantly longerthan T×E, suggesting that some genotypes have higher rates of meiotic


04_4453.qxd 10/20/05 3:06 PM Page 194

recombination than others. In some maps total genetic distances aredouble or even triple the size of the T×E map. Comparisons betweenintraspecific maps and interspecific maps have generally producedshorter maps in the latter than in the former (Gebhardt et al. 1991). Thiscan be explained by a decrease in crossing over frequencies between dis-tant genomes, compared to those that occur between chromosomes of thesame species. In the Prunus progenies studied, some of the maps sig-nificantly longer than T×E were those obtained with intraspecific crosses(peach, one of the apricot parents, and cherry), and the P. cerasifera par-ent of the P. cerasifera × ‘Felinem’ F1 progeny. Some of the shortest mapswere also obtained with interspecific populations, such as T×E and theBC1 of the cross between peach and P. ferganensis. Nevertheless, excep-tions were also very important, including all 4 almond maps, the P.davidiana map of the F1 with ‘Summergrand’, the peach ‘Akame’ ×‘Juseitou’ F2, and one of the parents of the apricot cross, which wereexpected to have longer maps, and the interspecific progenies ‘Garfi’ ×‘Nemared’ and ‘Felinem’ (a seedling of ‘Garfi’ × ‘Nemared’) and the F2

progeny of ‘Summergrand’ × P. davidiana, which were also expected toproduce longer maps. De Vicente and Tanksley (1991) found significantdifferences in recombination rates between male and female gametes intomato. If this happened in Prunus, the maps obtained with male andfemale individuals in F1 progenies would have different sizes. This wasnot the case in four of the five progenies studied, in all but the apricotF1 ‘Polonais’ × ‘Stark Early Orange’, but in this case the female parenthad a lower level of recombination, whereas in tomato the reduction ofrecombination occurred in the male gametes. The observed patternseems to fit with a model in which recombination rates would be asso-ciated to specific genotypes, more than to the distance between genomesor to sex. In the simple hypothesis that one or a few genes could beresponsible for the level of recombination of a certain individual, ourresults agree with a situation in which the alleles that increase recom-bination of these genes are absent or at a very low frequency in almondand present in cherry. Apricot and peach would be polymorphic forthese genes, and each individual would behave according to its geneticcomposition. Given that recombination is one of the driving forces ofplant breeding, characterization of its intensity in different genotypesmay be an important additional element in the selection of parents forspecific selection purposes.

The pattern of synteny observed in the species of the Prunus genus hasan exception. A reciprocal translocation was detected by Jáuregui et al.(2001), between ‘Nemared’ peach and ‘Garfi’ almond. Only seven link-age groups could be obtained in the map of the ‘Garfi’ × ‘Nemared’ F2


04_4453.qxd 10/20/05 3:06 PM Page 195

population, and one of these groups included markers placed on groups6 and 8 of T×E. The hypothesis of pseudolinkage between markers ofthese two chromosomes due to a reciprocal translocation was validatedwith cytogenetic studies and segregation of the semi-sterile and fully fer-tile individuals in the progeny. Although these data did not establishwhich of the parents (‘Garfi’ or ‘Nemared’) carried the translocation,indirect evidence points to ‘Nemared’ as the most probable translocatedgenotype (Jáuregui et al. 2001). ‘Nemared’ is a red-leaved genotype andthe breakpoint of the translocation was located in the same region of theGr/gr gene that determines the anthocyanin coloration of leaves, sug-gesting that there may be a relationship between the cytogenetic con-figuration and the morphology. Given that the ‘standard’ chromosomeconfiguration has been found in the rest of the almond and peach geno-types studied so far, it can be concluded that this chromosomalrearrangement is not characteristic of peach, but only present in someof its germplasm. The same reciprocal translocation was found in themap of ‘Felinem’ (Dirlewanger et al. 2004b), an expected result given thatthis rootstock is an offspring of ‘Garfi’ × ‘Nemared’, and in the ‘Akame’× ‘Juseitou’ peach F2 (Yamamoto et al. 2001a; Yamamoto, pers. comm.).Given that ‘Akame’ is a red-leaved genotype, this indicates that thetranslocation may occur in the group of red-leaved peaches. There aretwo more maps constructed with one red-leaved parent, the F2sNC174RL × ‘Pillar’ and ‘Lovell’ × ‘Nemared’ used by Chaparro et al.(1994) and Lu et al. (1998). Both maps are difficult to compare with oth-ers because they were constructed with dominant markers, but the addi-tion of a few SSR markers of linkage groups 6 and 8 would easilydemonstrate the presence of the translocation.

The general synteny between the genomes of Prunus and the existenceof a network of maps anchored with T×E allows positioning of all mark-ers, genes, or QTLs obtained in these maps in a common “consensus”map. Using the data available, it was possible to establish the positionof 28 major genes obtained in different species on a single map(Dirlewanger et al. 2004a). These major genes included 19 genes frompeach, 6 from almond or almond × peach crosses, 2 from apricot, andone from Myrobolan plum. A large number of QTLs from differentPrunus progenies, affecting characters such as disease resistance, fruitquality, blooming or fruit maturity times or tree architecture, have beenidentified (Testolin 2003). Those that are located in the populationswith maps anchored with T×E (Table 4.4) could be positioned in thePrunus “consensus” map using the same approach. Given the highmarker density of T×E and the possibility of finding additional markers


04_4453.qxd 10/20/05 3:06 PM Page 196

for specific regions using the information of homologous regions ofother maps, there is a high probability of finding markers sufficientlyclose to these genes or QTLs to be used in marker-assisted selection.

B. Between Apple and Pear

Although apple and pear belong to different genera, it is believed thatthey are genetically very close to each other because there are naturalinter-generic hybrids between them (Sax 1931; Weber 1964). In addition,a relatively large number of natural inter-generic hybrids have beenfound in the Maloideae, including Pyrus × Cydonia, Malus × Cydonia,Pyrus × Sorbus, Amelanchier × Sorbus, and Crataegus × Mespilus (Sax1931; Weber 1964). Yamamoto et al. (2001b) reported that SSR markersdeveloped in apple produced discrete amplified fragments in severalPyrus genotypes, indicating that apple SSRs could be applicable in pear.Nucleotide repeats were detected in amplified fragments in pear, and theDNA sequence of flanking regions in apple was highly conserved in pear,indicating that SSR markers are good tools to compare genetic linkagemaps obtained from different species as well as different genera of theMaloideae. Liebhard et al. (2002) noted that apple SSRs successfullyamplified in species of other Maloideae genera (Amelanchier,Cotoneaster, Crataegus, Cydonia, Mespilus, Pyrus, and Sorbus). TheSSR markers developed in apple and pear have been utilized as a reli-able tool for identifying quince varieties (Yamamoto et al. 2004b). Thirty-nine and 29 SSR markers derived from apple produced segregating lociin the genetic maps of ‘Bartlett’ and ‘Housui’, respectively (Yamamotoet al. 2004a). Sixty-six apple SSRs were also mapped in a genetic mapof the European pear cultivar ‘La France’ constructed from the three-wayinterspecific hybrid progeny of ‘Shinsei’ × 282-12 (‘Housui’ × ‘LaFrance’) (T. Yamamoto, unpubl. data). When the pear maps of ‘Bartlett’,‘Housui’, and ‘La France’ were compared with those of ‘Fiesta’ and ‘Dis-covery’, all pear linkage groups could be successfully aligned to theapple reference map by at least one apple SSR, suggesting that positionsand linkages of SSR loci were well conserved between pear and apple.

As Fig. 4.1 shows, on linkage groups 10, 12, 14, and 15, there are 8, 7,7, and 5 SSRs, respectively, located in both maps of apple and pear. Posi-tions, order, and linkage of SSR loci found in genetic maps of apple andpear were almost completely conserved in these 4 linkage groups. Theself-incompatibility locus (S locus) was mapped to linkage group 17 inJapanese and European pears as well as in apple (Yamamoto et al.2004a). In all, these results indicate a high level of conservation between


04_4453.qxd 10/20/05 3:06 PM Page 197

the pear and apple genomes. This information may be applicable toother Maloideae genera and will help to advance genome research inlesser-known fruit tree species such as quince, loquat, and medlar.

About 10–20% of SSR markers in apple and pear are multi-locus(Liebhard et al. 2002; Liebhard et al. 2003a; Yamamoto et al. 2004a).Maliepaard et al. (1998) identified several homeologous linkage groupsof apple using the markers detected by duplicated RFLPs. Similarly,Liebhard et al. (2002, 2003a) pointed out duplication patterns of multi-locus SSRs in the linkage group pairs 1-3, 1-7, 4-12, 5-10, 8-15, 9-17, 12-13, and 12-14 of apple. In pear, duplication of the linkage group pairs1-3, 2-15, 5-10, 8-15, 9-17, 10-17, 12-14, and 13-16 were revealed bymulti-locus SSRs (Yamamoto et al. 2004a). Duplications of linkage


CH02a08

CH01f12CH02c11

CH04g09

CH01f07aCH02b03bMS02a01

MS06g03

L10A

CH02a08

CH01f12

CH02c11

CH04g09

CH01f07aCH02b03bMS02a01MS06g03

L10P

CH05d04

CH04g04CH05g07CH05d11

CH04d02CH01f02CH03c02

L12A

CH05d04

CH04g04CH05g07CH05d11

CH04d02CH01f02CH03c02

L12P

CH05g07CH01g05CH04f06CH03d08CH05g11CH04c07CH05d03

L14A

CH05g07

CH01g05CH04f06CH03d08CH05g11CH04c07CH05d03

L14P

NZ02b1CH05a02

CH01d08

CH02d11

CH02c09

L15A

NZ02b1CH05a02

CH01d08

CH02d11

CH02c09

L15P

50 c

M

Fig. 4.1. Comparison between linkage groups 10, 12, 14, and 15 of apple and pear.Groups are labelled with L followed by the group number and “A” for apple or “P” for pear.Linkage groups of apple are from the genetic map of ‘Discovery’ described in Liebhard etal. (2003a). Linkage groups of pear are from an integrated map of ‘Bartlett’, ‘Housui’, and‘La France’ (Yamamoto et al. 2004a, unpublished data). Anchor SSRs are indicated by thedotted lines.

04_4453.qxd 10/20/05 3:06 PM Page 198

groups 1-3, 5-10, 8-15, 9-17, and 12-14 were observed in both apple andpear.

C. Between Apple and Prunus

Data for the comparison of these two genomes are limited to the 30common loci (24 RFLPs and 6 isozymes) between the Prunus T×E andthe apple ‘Prima’ × ‘Fiesta’ maps (Dirlewanger et al. 2004a). A compar-ison between the three Prunus linkage groups having three or moreanchor markers with apple linkage groups is shown in Fig. 4.2. Four


L16L13

L8

AG53a

LY5a

LY5b

Lap-2, MC022

MC001b

MC041aMC041b

MC001a

Aat-2

LY16a

LY21a

G3 L9 L17MC115

MC115bMC115a

MC038A

MC038bMC038a

(Aat-2) Aat-1

MC007

MC007a

Me-1

G4

L10

L5

MC028BMC028a

MC030A MC030b

MC030a

MC024A MC024aMC024b

MC028b

L2

L1, L7

G1MC013

AG53

LY5B

MC001

Pgm-2

Lap-2

LY37, MC022

(Aat-1)

LY16A

LY21

L15

L4

10 cM

Fig. 4.2. Comparison between Prunus (Joobeur et al. 1998) and apple (Maliepaard et al.1998) linkage maps. Only the position of anchor loci is shown. Linkage groups in Prunusare labelled G, and apple groups L, followed by a number. The positions of markers inparentheses in Prunus were inferred from other maps. Marker positions in apple wereobtained using the maps of both parents of the F1 cross ‘Prima’ × ‘Fiesta’. Two paralleloblique lines indicate that only a fragment of the linkage group is included. Arrows point-ing to the left in the Prunus map are anchors to markers located in the indicated linkagegroups of the apple map. Reproduced with permission from Dirlewanger et al. (2004) Com-parative mapping and marker assisted selection in Rosaceae fruit crops. Proc. Natl. Acad.Sci. (USA) 101:9891–9896 (copyright (2004) National Academy of Sciences, U.S.A.).

04_4453.qxd 10/20/05 3:06 PM Page 199

more Prunus groups had anchor points with the apple map, three ofthem with two markers each: G2, corresponding to apple groups L3 andL11, G8, to L5, L3 and L10 and G7 to L14, and one with one marker, G5,which had its homologue in apple group L6 (Joobeur 1998). For the link-age groups with more common markers, the position of most lociappears colinear and the distances between contiguous loci are similar,suggesting that the synteny between the chromosomes compared isimportant. G3 and G7 are homologous to two apple linkage groups each,as expected if they correspond to two homeologous chromosomes. Thecomparison of G1 is especially interesting because its upper part corre-sponds to two homeologous apple groups (L13 and L16), whereas thelower part is syntenic to one more apple group (L8), suggesting thateither two of the chromosomes of the ancestor species of apple andPrunus fused in the Prunus lineage, or one chromosome of this ances-tor split into two in the Malus lineage. This agrees with the cytogeneticobservation that apple does not have the large chromosome observed inPrunus (Bouvier et al. 2000).

Recent molecular genetic studies refuted the hypothesis that theallopolyploid genome of the Maloideae (x = 17) included one Prunoideae(x = 8) and one Spiraeoideae (x = 9) genome, but supported autopoly-ploidy or hybridization between closely related members of a single lin-eage, with species of the Spiraeoideae subfamily being the most probableparental lineages (Morgan et al. 1994; Evans and Campbell 2002). Phy-logenetic analysis of the rbcL gene sequence does not provide closelinks between Maloideae and Prunoideae but between Maloideae and some genera of Spiraeoideae (Morgan et al. 1994). Based on GBSSI(granule-bound starch synthase, waxy) genes, Evans and Campbell(2002) showed that the subfamily Maloideae originated from polyploidyinvolving only members of a lineage that contained the ancestors of Gillenia, of the Spiraeoideae. If one of the differences between the genomes of Prunoideae and Spiraeoideae is that the long chromo-some of the former corresponds to two in the latter, our observation thatthe long G1 group of Prunus appears to be split into two in apple is inagreement with the origin of the Maloideae genome being composed oftwo Spiroideae genomes without the inclusion of a Prunoideae genome.

The level of transferability of SSRs between Maloideae and Prunoi-deae was rather low, suggesting that these markers are inadequate formap comparisons between species of these two subfamilies. Cipriani etal. (1999) found that only 18% of peach SSRs were amplified in apple.Yamamoto et al. (2004a) noted that only about one-tenth of the PrunusSSRs could be mapped in maps of ‘Bartlett’ and ‘Housui’. Only one out


04_4453.qxd 10/20/05 3:06 PM Page 200

of 15 apple SSR markers was transferable to Prunoideae (Liebhard et al.2002).

D. Between Prunus and Arabidopsis

Most of the probes used for RFLP mapping in the Prunus T×E referencemap have been obtained with probes of known sequence. For some ofthe RFLPs of this map (detecting 111 loci), Arabidopsis probes with ahigh level of homology with rice sequences were used, and for others weused probes mostly from almond, peach, and other Rosaceae DNAlibraries, some of which (detecting 116 additional loci) have a high levelof sequence homology (TBLASTX value <10–15) with Arabidopsissequences. Using these 227 loci of the Prunus genome (average densityof 2.6 cM/locus), 703 corresponding homologous loci were found in theArabidopsis sequence (Dominguez et al. 2003).

For the establishment of syntenic regions between the two species, thefollowing criteria were used: (1) three or more homologous markers hadto be located within 1% of the Prunus map distance (6 cM) and within1% of the Arabidopsis genome (1.2 Mb) and (2) more markers could beadded to this region if its density of homologous markers was equal orbelow 3 markers/cM in Prunus and 3 markers/1.2 Mb in Arabidopsis andthere were no gaps larger than 1% of either genome. Thirty-seven regionsmeeting these criteria were detected (Dominguez et al. 2003), distributedalong all chromosomes of both species and covering 23% of the Prunusand 17% of the Arabidopsis genomes. The largest of them (25 cM) wasin a region of G2 that included 13 loci that corresponded to a segment(5.3 Mbp) of chromosome 5 of Arabidopsis with 16 markers.

The distribution of Prunus/Arabidopsis syntenic regions indicatesthat some degree of synteny can still be recognized between these tworemotely related genomes, but that this synteny is incomplete and a largenumber of chromosomal rearrangements have occurred. Sequencing ofArabidopsis revealed that this simple genome had a high level of dupli-cation from several remote polyploidisation events (Blanc et al. 2000;Vision et al. 2000), which suggested that a similar pattern could befound in other species. Some regions of Arabidopsis (chromosomes 1,2, 3, and 5) identified several overlapping Prunus fragments, suggestingthat these are some of the duplicate regions of the Prunus genome(Dominguez et al. 2003).

At a high-resolution level, the available data suggest that specificregions of the peach genome maintain a very limited microsynteny withthe Arabidopsis genome (Georgi et al. 2003; B. Sosinski, unpubl.). These


04_4453.qxd 10/20/05 3:06 PM Page 201

initial studies suggest that substantial genome rearrangements haveoccurred in very small genomic windows, thus limiting the value ofinterfamily comparative genomics as a tool for gene discovery. However,within the genus Prunus, the high level of genome preservation at themacrosynteny scale suggests that the peach genome will serve as ananchor genome for identification of important genes in other species ofthe genus.

IV. OTHER GENETIC RESOURCES OF INTEREST FOR MAP COMPARISON

Genomics and genetics data from the main Rosaceae species are rapidlyaccumulating. These data are essential for comparative mapping, posi-tional cloning, gene discovery, and the analysis of gene function. Theiruse will lead to a better understanding of the Rosaceae genome in theimmediate future. Three of the most important resources currently inprogress are summarized in the following paragraphs.

A. The Genome Database for Rosaceae (GDR)

All the structural and functional genomics resources are incorporated inthe GDR website currently under construction at Clemson,www.genome.clemson.edu/gdr/ (Jung et al. 2004). This website is a cen-tralized, curated, and integrated repository for worldwide Rosaceaegenomics data, including genetic maps, physical maps, EST data repos-itories, germplasm information, and interactive search and query toolsfor data analysis.

B. The Peach Physical Map

A number of large-insert libraries have been produced for most of theimportant species of the Rosaceae. Bacterial artificial chromosome (BAC)libraries have been constructed in peach (Georgi et al. 2002), apricot(Vilanova at el. 2003b), myrobalan plum (Claverie et al. 2004), and apple(Vinatzer et al. 1998; Xu et al. 2002) and are under construction in otherspecies such as cherry, strawberry, and rose. Utilizing the peach BAClibrary resources, the International Rosaceae Mapping Project (IRMP) isconstructing a complete physical map of the peach genome anchored onthe reference Prunus genetic map (Joobeur et al. 1998). BAC fingerprintsof 25,000 BACs (20,000 from a BAC library from the rootstock cultivar‘Nemared’ and 5,000 from another BAC library from a haploid plant of


04_4453.qxd 10/20/05 3:06 PM Page 202

cultivar ‘Lovell’) have been obtained, from which approximately 20,000have been used to construct an initial physical map.

At this juncture, the framework map is composed of around 1,000 con-tigs containing approximately 8,000 clones. The current estimate ofgenome coverage in this map is approximately 80% of the peach genomein high-confidence contigs. Current efforts are directed at merging con-tig ends to obtain chromosome length BAC tiling paths. As the mapincludes marker hybridization data from the T×E general Prunus geneticmap (210 low-copy probes of mapped RFLP markers have beenhybridised to the BAC libraries), the developing physical map is directlyanchored to the genetic map.

C. EST Functional Genomics Database Development

The IRMP in cooperation with the bioinformatics group of the GDR isdeveloping a candidate gene database for the Rosaceae. This databaseexceeds 200,000 EST sequences from many of the key species in theRosaceae. Unigene sets are currently under development for peach,apple, strawberry, and for the Rosaceae as a whole. The EST data for thefamily is compiled weekly and housed in the GDR.

Rosaceae unigenes are being mapped to the physical map of peach.This physically mapped EST resource will provide candidate genes formarked regions of the Prunus maps containing traits of interest andserve as a substrate for microsynteny analysis of target genome regions.From the initial fruit unigene set, we have completed hybridizing inexcess of 3,200 peach fruit unigenes onto the ‘Nemared’ BAC library, ofwhich, data on 1,700 ESTs have been annotated and BACs fingerprinted.From this annotated set, 184 ESTs have been located directly on thePrunus reference map through common hybridization of mapped mol-ecular markers and ESTs. BACs have been identified in the ‘Nemared’library for all but around 15% of these ESTs. Initial hybridizations ofaround 100 ESTs, from these remaining orphan ESTs, on the haploid‘Lovell’ BAC library have been 60% successful. Thus, upon completionof the physical map, virtually all EST locations will be identified.

V. FUTURE PROSPECTS

A decade after the publication of the first maps of Rosaceae species, theapple map of Hemmat et al. (1994) and the peach map of Chaparro et al.(1994), the amount of information available on the genome of this fam-ily has grown enormously. The main advances are: the saturated or


04_4453.qxd 10/20/05 3:06 PM Page 203

nearly saturated maps constructed with codominant and transferablemarkers in three key genera, Prunus, Malus, and Fragaria; the estab-lishment of the synteny between Prunus species and between Malus andPyrus; the development of important genomic tools, mainly in peach andapple (BAC libraries and EST collections); the construction of a peachphysical map anchored in the genetic linkage map and with the positionof an increasing number of transcribed DNA sequences known; and the creation of a Rosaceae database that allows access to these data bythe scientific community. Other important steps forward have been therecent map-based cloning of the Vf gene of apple, conferring resistanceto apple scab (Belfanti et al. 2004), and the progress towards the sequenc-ing of the aphid resistance gene (Sd-1) of apple (Cevik and King 2002)and the Ma gene of nematode resistance in myrobalan plum (Claverie etal. 2004).

Rosaceae synteny analysis is only at its beginning. Some of the mostimportant map comparisons remain to be done, particularly the com-parison between species of the three Rosaceae subfamilies, from whichPrunus and Malus/Pyrus and Prunus and Fragaria seem good choices.Even though they are in the same subfamily and share the same basicchromosome number, the comparison of the genomes of rose, straw-berry, and blackberry is a necessary step for a global understanding ofthe pattern of synteny of the family. While SSR development has beencrucial in the last years for map comparisons within the subfamily,these markers are not transferable enough for inter-subfamily compar-isons and other markers should be used. RFLPs (a few hundred aremapped in Prunus), SNPs, CAPSs, indels or other markers, based ontranscribed DNA sequences using the growing collections of ESTs (manyof them placed on the peach physical map) of various Rosaceae, orbased on Rosaceae homologues of sequences well characterized in otherspecies and expected to be single or low copy in Prunus, such as the COStomato sequences (Fulton et al. 2002), could be adequate markers for thispurpose. While the comparison of the genome sequence of specific chro-mosome regions in different species of the same family has generallydetected a high degree of conservation (Bancroft 2001), microsyntenyanalysis has not been attempted between members of different Rosaceaesubfamilies, and would provide a different and complementary level ofgenome similarity information, useful, among other applications, indetermining the extent to which the advances obtained in one modelspecies of this family can be applied to the remaining.

Many morphological single-gene markers have been positioned inmaps of different Rosaceae, and results from QTL analyses are startingto emerge, mainly in apple (Liebhard et al. 2003b; Liebhard et al. 2003c)


04_4453.qxd 10/20/05 3:06 PM Page 204

and Prunus (Etienne et al. 2002; Quilot et al. 2004). It is expected thatin the coming years more studies will be published and the inheritanceof many quantitative and qualitative characters of interest will be betterknown. The in-depth knowledge of the synteny between differentRosaceae may be extremely helpful in designing strategies, at the wholefamily level, to localize homologous regions containing genes/QTLs ofinterest, to find allelic variation, to identify candidate genes located ata target region or to find tightly linked markers to a gene/QTL appro-priate for marker-assisted selection. For this purpose, the integration ofthese data into the GDR database is required.

The total or partial sequence of one genome of the Rosaceae would fos-ter genetic research in this family, and lead to important practical results.As evidenced by the macro- and micro-synteny comparisons with Ara-bidopsis, the genome sequence of this model species can only be usedto a limited extend for understanding the genome of the Rosaceae. Dueto the important developments of genome research achieved in recentyears and currently in progress, peach stands out as a good candidate forthis purpose.

LITERATURE CITED

Abbott, A. G., A. C. Lecouls, Y. Wang, L. Georgi, R. Scorza, and G. Reighard. 2002. Peach:the model genome for Rosaceae genomics. Acta Hort. 592:199–209.

Ahn, S., and S. D. Tanksley. 1993. Comparative linkage maps of the rice and maizegenomes. Proc. Natl. Acad. Sci. (USA) 90:7980–7984.

Akiyama, Y., Y. Yamamoto, N. Ohmido, M. Ohshima, and K. Fukui. 2001. Estimation ofthe nuclear DNA content of strawberries (Fragaria spp.) compared with Arabidopsisthaliana by using dual-step flow cytometry. Cytologia 66:431–436.

Alston, F. H., K. L. Phillips, and K. M. Evans. 2000. A Malus gene list. Acta Hort.538:561–570.

Aranzana, M. J., A. Pineda, P. Cosson, E. Dirlewanger, J. Ascasibar, G. Cipriani, C. D. Ryder,R. Testolin, A. Abbott, G. J. King, A. F. Iezzoni, and P. Arús. 2003. A set of simple-sequence repeat (SSR) markers covering the Prunus genome. Theor. Appl. Genet.106:819–825.

Arumuganathan, K., and E. D. Earle. 1991. Nuclear DNA content of some important plantspecies. Plant Mol. Biol. Rep. 9:208–218.

Baird, W. V., A. S. Estager, and J. K. Wells. 1994. Estimating nuclear DNA content in peachand related diploid species using laser flow cytometry and DNA hybridization. J. Am.Soc. Hort. Sci. 199:1312–1316.

Ballester, J., R. Socias i Company, P. Arús, and M. C. de Vicente. 2001. Genetic mappingof a major gene delaying blooming time in almond. Plant Breed. 120:268–270.

Bancroft, I. 2001. Duplicate and diverge: the evolution of plant genome microstructure.Trends Genet. 17:89–93.

Beaver, J. A., and A. F. Iezzoni. 1993. Allozyme inheritance in tetraploid sour cherry(Prunus cerasus L.). J. Am. Soc. Hort. Sci. 118:873–877.


04_4453.qxd 10/20/05 3:06 PM Page 205

Belfanti, E., E. Silfverberg-Dilworth, S. Tartarini, A. Patocchi, M. Barbieri, J. Zhu, B. A.Vinatzer, L. Gianfranceschi, C. Gessler, and S. Sansavini. 2004. The HcrVf2 gene froma wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad.Sci. (USA) 101:886–890.

Blanc, G., A. Barakat, R. Guyot, R. Cooke, and M. Delseny. 2000. Large duplications in theArabidopsis thaliana genome. Plant Cell 12:1093–1101.

Bliss, F. A., S. Arulsekar, M. R. Foolad, V. Becerra, A. M. Gillen, M. L. Warburton, A. M.Dandekar, G. M. Kocsisne, and K. K. Mydin. 2002. An expanded genetic linkage mapof Prunus based on an interspecific cross between almond and peach. Genome45:520–529.

Boskovic, R., and K. R. Tobutt. 1998. Inheritance and linkage relationships of isoenzymesin two interspecific cherry progenies. Euphytica 103:273–286.

Bouvier, L., Y. Lespinasse, and M. Schuster. 2000. Karyotype analysis of a haploid plantof apple (Malus domestica). Acta Hort. 538:321–324.

Brown, S. K. 1992. Genetics of apple. Plant Breed. Rev. 9:333–366.Cevik, V., and G. J. King, 2002. Resolving the aphid resistance locus Sd-1 on a BAC con-

tig within a sub-telomeric region of Malus linkage group 7. Genome 45:939–945.Claverie, M., E. Dirlewanger, P. Cosson, N. Bosselut, A. C. Lecouls, R. Voisin, M. Klein-

hentz, B. Lafargue, M. Caboche, B. Chalhoub, and D. Esmenjaud. 2004. High-resolutionmapping and chromosome landing at the root-knot nematode resistance locus Ma fromMyrobalan plum using a large-insert BAC DNA library. Theor. Appl. Genet. 109:1318–1327.

Chaparro, J. X., D. J. Werner, D. O’Malley, and R. R. Sederoff. 1994. Targeted mapping andlinkage analysis of morphological isozyme, and RAPD markers in peach. Theor. Appl.Genet. 87:805–815.

Choi, H. K., J. H. Mun, D. J. Kim, H. Zhu, J. M. Baek, J. Mudge, B. Roe, N. Ellis, J. Doyle,G. B. Kiss, N. D. Young, and D. R. Cook. 2004. Estimating genome conservation betweencrop and model legume species. Proc. Natl. Acad. Sci. (USA) 101:15289–15294.

Cipriani, G., G. Lot, W. G. Huang, M. T. Marrazzo, E. Peterlunger, and R. Testolin. 1999.AC/GT and AG/CT microsatellite repeats in peach (Prunus persica (L) Batsch): Isola-tion, characterisation and cross-species amplification in Prunus. Theor. Appl. Genet.99:65–72.

Conner, P. J., S. K. Brown, and N. F. Weeden. 1997. Randomly amplified polymorphicDNA-based genetic linkage maps of three apple cultivars. J. Am. Soc. Hort. Sci. 122:350–359.

Corredor E., M. Román, E. García, E. Perera, P. Arús, and T. Naranjo. 2004. Physical map-ping of rDNA genes enables to establish the karyotype of almond. Ann. Appl. Biol.144:219–222.

Crespel, L., M. Chirollet, C. E. Durel, D. Zhang, J. Meynet, and S. Gudin. 2002. Mappingqualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theor.Appl. Genet. 105:1207–1214.

Da Silva, J. A. G., M. E. Sorrels, W. L. Burnquist, and S. D. Tanksley. 1993. RFLP linkagemap and genome analysis of Saccharum spontaneum. Genome 36:782–791.

Davis, T. M., and H. Yu. 1997. A linkage map of the diploid strawberry Fragaria vesca. J.Hered. 88:215–221.

Debener, T., and L. Mattiesch. 1999. Construction of a genetic linkage map for roses usingRAPD and AFLP markers. Theor. Appl. Genet. 99:891–899.

Dettori, M. T., R. Quarta, and I. Verde. 2001. A peach linkage map integrating RFLPs, SSRs,RAPDs, and morphological markers. Genome 44:783–790.


04_4453.qxd 10/20/05 3:06 PM Page 206

De Vicente, M. C., and S. D. Tanksley. 1991. Genome-wide reduction in recombination ofbackcross progeny derived from male versus female gametes in an interspecific crossof tomato. Theor. Appl. Genet. 83:173–178.

Devos, K. M., and M. D. Gale. 2000. Genome relationships: the grass model in currentresearch. Plant Cell 12:637–646.

Dickson, E. E., K. Arumuganathan, S. Kresovich, and J. J. Doyle. 1992. Nuclear DNA con-tent variation within the Rosaceae. Am. J. Bot. 79:1081–1086.

Dirlewanger, E., P. Cosson, M. Tavaud, M. J. Aranzana, C. Poizat, A. Zanetto, P. Arús, andF. Laigret. 2002. Development of microsatellite markers in peach (Prunus persica (L.)Batsch) and their use in genetic diversity analysis in peach and sweet cherry (Prunusavium L.). Theor. Appl. Genet. 105:127–138.

Dirlewanger, E., E. Graziano, T. Joobeur, F. Garriga-Calderé, P. Cosson, W. Howad, and P.Arús. 2004a. Comparative mapping and marker assisted selection in Rosaceae fruitcrops. Proc. Natl. Acad. Sci. (USA) 101:9891–9896.

Dirlewanger, E., P. Cosson, W. Howad, G. Capdevill, N. Bosselu, M. Claverie, R. Voisin,C. Poizat, B. Lafarge, O. Baron, F. Laigret, M. Kleinhentz, P. Arús, and D. Esmenjaud.2004b. Microsatellite genetic linkage maps of Myrobalan plum and an almond-peachhybrid—Location of root-knot nematode resistance genes. Theor. Appl. Genet.109:827–838.

Diwan, N., J. H. Bouton, G. Kochert, and P. B. Cregan. 2000. Mapping of simple-sequencerepeat (SSR) DNA markers in diploid and tetraploid alfalfa. Theor. Appl. Genet.101:165–172.

Doganlar, S., A. Frary, M.-C. Daunay, R. N. Lester, and S. D. Tanksley. 2003. A compara-tive genetic map of eggplant and its implication for genome evolution of the Solanaceae.Genetics 161:1697–1711.

Dominguez, I., E. Graziano, C. Gebhardt, A. Barakat, S. Berry, P. Arús, M. Delseny, and S.Barnes. 2003. Plant genome archaeology: evidence for conserved ancestral chromosomesegments in dicotyledonous plant species. Plant Biotech. J. 1:91–99.

Dunford, R. P., N. Kurata, D. A. Laurie, T. A. Money, Y. Minobe, and G. Moore. 1995. Con-servation of fine-scale DNA marker order in the genomes of rice and the Triticeae.Nucleic Acids Res. 23:2724–2728.

Etienne, C., C. Rothan, A. Moing, C. Plomion, C. Bodenes, L. S. Dumas, P. Cosson, V.Pronier, R. Monet, and E. Dirlewanger. 2002. Candidate genes and QTLs for sugar andorganic acid content in peach (Prunus persica (L.) Batsch). Theor. Appl. Genet. 105:145–159.

Evans, R. C., and C. S. Campbell. 2002. The origin of the apple subfamily (Maloideae;Posaceae) is clarified by DNA sequence data from duplicated GBSSI genes. Am. J. Bot.89:1478–1484.

Foolad, M. R., S. Arulsekar, V. Becerra, and F. A. Bliss. 1995. A genetic map of Prunusbased on an interspecific cross between peach and almond. Theor. Appl. Genet. 91:262–269.

Foulongne, M., T. Pascal, P. Arús, and J. Kervella. 2003. The potential of Prunus davidi-ana for introgression into peach (Prunus persica (L.) Batsch) assessed by comparativemapping. Theor. Appl. Genet. 107:227–238.

Fulton, T. M., R. van der Hoeven, N. T. Eannetta, and S. D. Tanksley. 2002. Identification,analysis, and utilization of conserved ortholog set markers for comparative genomicsin higher plants. Plant Cell 14:1457–1467.

Gebhardt, C., E. Ritter, A. Barone, T. Debener, B. Walkemeier, U. Schachtschabel, H. Kauf-mann, R. D. Thompson, M. W. Bonierbale, M. W. Ganal, S. D. Tanksley, and F. Salamini.


04_4453.qxd 10/20/05 3:06 PM Page 207

1991. RFLP maps of potato and their alignment with the homoeologous tomato genome.Theor. Appl. Genet. 83:49–57.

Georgi, L. L., Y. Wang, D. Yvergniaux, T. Ormsbee, M. Iñigo, G. Reighard, and A. G.Abbott. 2002. Construction of a BAC library and its application to the identification ofsimple sequence repeats in peach (Prunus persica (L.) Batsch). Theor. Appl. Genet.105:1151–1158.

Georgi, L. L., L. Wang, G. L. Reighard, L. Mao, R. A. Wing, and A. G. Abbott. 2003. Com-parison of peach and Arabidopsis genomic sequences: fragmentary conservation ofgene neighborhoods. Genome 46:268–276.

Gianfranceschi, L., N. Seglias, R. Tarchini, M. Komjac, and C. Gessler. 1998. Simplesequence repeats for the genetic analysis of apple. Theor. Appl. Genet. 96:1069–1076.

Graham, J., K. Smith, K. MacKenzie, L. Jorgenson, C. Hackett, and W. Powell. 2004. Theconstruction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus)based on AFLPs, genomic-SSR and EST-SSR markers. Theor. Appl. Genet. (in press).

Grattapaglia, D., and R. Sederoff. 1994. Genetic linkage maps of Eucalyptus grandis andEucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers.Genetics 137:1121–1137.

Hemmat, M., N. F. Weeden, A. G. Manganaris, and D. M. Lawson. 1994. Molecular markerlinkage map for apple. J. Hered. 85:4–11.

Hemmat, M., N. F. Weeden, and S. K. Brown. 2003. Mapping and evaluation of Malus ×domestica microsatellites in apple and pear. J. Am. Soc. Hort. Sci. 128:515–520.

Hesse, C. O. 1975. Peaches. p. 285–335. In: J. Janick and J. N. Moore (eds.), Advances infruit breeding. Purdue Univ. Press, West Lafayette, Indiana.

Hokanson, S. C., A. K. Szewc-McFadden, W. F. Lamboy, and J. R. McFerson. 1998. Micro-satellite (SSR) markers reveal genetic identities, genetic diversity and relationships ina Malus × domestica Borkh. core subset collection. Theor. Appl. Genet. 97:671–683.

Hormaza, J. I. 2002. Molecular characterization and similarity relationships among apri-cot (Prunus armeniaca L.) genotypes using simple sequence repeats. Theor. Appl.Genet. 104:321–328.

Hurtado, M., C. Romero, S. Vilanova, A. Abbott, G. Llácer, and M. Badenes. 2002. Geneticlinkage maps of two apricot cultivars (Prunus armeniaca L.), and mapping of PPV(sharka) resistance. Theor. Appl. Genet. 105:182–191.

Iketani, H., K. Abe, T. Yamamoto, K. Kotobuki, Y. Sato, T. Saito, O. Terai, N. Matsuta, andT. Hayashi. 2001. Mapping of disease-related genes in Japanese pear using a molecu-lar linkage map with RAPD markers. Breed. Sci. 51:179–184.

Janick, J., J. N. Cummings, S. K. Brown, and M. Hemmat. 1996. Apples. p. 1–77. In: J. Jan-ick and N. J. Moore (eds.), Fruit breeding, Vol. I: Tree and tropical fruits. Wiley, NewYork.

Jáuregui, B., M. C. de Vicente, R. Messeguer, A. Felipe, A. Bonnet, G. Salesses, and P. Arús.2001. A reciprocal translocation between ‘Garfi’ almond and ‘Nemared’ peach. Theor.Appl. Genet. 102:1169–1176.

Jones, J. K. 1976. Strawberry (Fragaria ananassa). p. 237–242. In: N. W. Simmonds (ed.),Evolution of crop plants. Longman, New York.

Joobeur, T. 1998. Construcción de un mapa de marcadores moleculares y análisis genéticode caracteres agronómicos en Prunus. Ph.D. thesis. Univ. Lleida, Spain.

Joobeur, T., M. A. Viruel, M. C. de Vicente, B. Jáuregui, J. Ballester, M. T. Dettori, I. Verde,M. J. Truco, R. Messeguer, I. Batlle, R. Quarta, E. Dirlewanger, and P. Arús. 1998. Con-struction of a saturated linkage map for Prunus using an almond × peach F2 progeny.Theor. Appl. Genet. 97:1034–1041.


04_4453.qxd 10/20/05 3:06 PM Page 208

Joobeur, T., N. Periam, M. C. de Vicente, G. King, and P. Arús. 2000. Development of a sec-ond generation linkage map for almond using RAPD and SSR markers. Genome43:649–655.

Jung, S., C. Jesudurai, M. Staton, Z. Du, S. Ficklin, I. Cho, A. Abbott, J. Tomkins, and D.Main. 2004. BMC Bioinformatics 5:130.

Knight, R. L. 1963. Abstract bibliography of fruit breeding and genetics to 1960: Malus andPyrus. Tech. Commun. Commonw. Bur. Hort. Plant. Crops 29.

Kovanda, M. 1965. On the generic concepts in the Maloideae. Preslia (Praha) 37:27–34.Lambert, P., L. S. Hagen, P. Arús, and J. M. Audergon. 2004. Genetic linkage maps of two

apricot cultivars (Prunus armeniaca L.) compared with the almond Texas × peach Ear-lygold reference map for Prunus. Theor. Appl. Genet. 108:1120–1130.

Lander, E. S., P. Green, J. Abrahamson, A. Barlow, M. J. Daly, S. E. Lincoln, and L. New-burg. 1987. MAPMAKER: An interactive computer package for constructing primarygenetic linkage maps of experimental and natural populations. Genomics 1:174–181.

Lecerteau-Köhler, E., G. Guérin, F. Laigret, and B. Denoyes-Rothan. 2003. Characterizationof mixed disomic and polysomic inheritance in the octoploid strawberry (Fragaria ×ananassa) using AFLP mapping. Theor. Appl. Genet. 107:619–628.

Liebhard, R., L. Gianfranceschi, B. Koller, C. D. Ryder, R. Tarchini, E. Van De Weg, andC. Gessler. 2002. Development and characterisation of 140 new microsatellites in apple(Malus × domestica Borkh.). Mol. Breed. 10:217–241.

Liebhard, R., B. Koller, L. Gianfranceschi, and C. Gessler. 2003a. Creating a saturated ref-erence map for the apple (Malus × domestica Borkh.) genome. Theor. Appl. Genet.106:1497–1508.

Liebhard, R., M. Kellerhals, W. Pfammatter, M. Jertmini, and C. Gessler. 2003b. Mappingquantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol. Biol.52:511–526.

Liebhard, R., B. Koller, A. Patocchi, M. Kellerhals, W. Pfammatter, M. Jertmini, and C.Gessler. 2003c. Mapping quantitative field resistance against apple scab in a ‘Fiesta’ ×‘Discovery’ progeny. Phytopathology 93:493–501.

Lu, Z. X., B. Sosinski, G. L. Reighard, W. V. Baird, and A. G. Abbott. 1998. Constructionof a genetic linkage map and identification of AFLP markers for resistance to root-knotnematodes in peach rootstocks. Genome 41:199–207.

Luby, J. J. 2003. Taxonomic classification and brief history. p. 1–14. In: D. C. Ferree andI. J. Warrington (eds.), Apples: Botany, production and uses. CABI Publi., Cambridge, MA.

Lukens, L., F. Zou, D. Lydiate, I. Parkin, and T. Osborn. 2003. Comparison of Brassica oler-acea genetic map with the genome of Arabidopsis thaliana. Genetics 164:359–372.

Maliepaard, C., F. H. Alston, G. van Arkel, L. M. Brown, E. Chevreau, F. Dunemann, K.M. Evans, S. Gardiner, P. Guilford, A. W. van Heusden, J. Janse, F. Laurens, J. R. Lynn,A. G. Manganaris, A. P. M. den Nijs, N. Periam, E. Rikkerink, P. Roche, C. Ryder, S.Sansavini, H. Schmidt, S. Tartarini, J. J. Verhaegh, M. Vrielink-van Ginkel, and G. J.King. 1998. Aligning male and female linkage maps of apple (Malus pumila Mill.)using multi-allelic markers. Theor. Appl. Genet. 97:60–73.

Milbourne, D., R. C. Meyer, A. J. Collins, L. D. Ramsay, C. Gebhardt, and R. Waugh. 1998.Isolation, characterisation and mapping of simple sequence repeat loci in potato. Mol.Gen. Genet. 259:233–245.

Monet, R., A. Guye, M. Roy, and N. Dachary. 1996. Peach Mendelian genetics: a shortreview and new results. Agronomie 16:321–329.

Morgan, D. R., D. E. Soltis, and K. R. Robertson. 1994. Systematic and evolutionary impli-cations of rbcL sequence variation in Rosaceae. Am. J. Bot. 81:890–903.


04_4453.qxd 10/20/05 3:06 PM Page 209

Quilot, B., B. H. Wu, J. Kervella, M. Génard, M. Foulongne, and K. Moreau. 2004. QTLanalysis of quality traits in an advanced backcross between Prunus persica cultivars andthe wild relative species P. davidiana. Theor. Appl. Genet. 109:884–897.

Rajapakse, S., L. E. Bethoff, G. He, A. E. Estager, R. Scorza, I. Verde, R. E. Ballard, W. V.Baird, A. Callahan, R. Monet, and A. G. Abbott. 1995. Genetic linkage mapping inpeach using morphological, RFLP and RAPD markers. Theor. Appl. Genet. 90:503–510.

Rajapakse, S., D. H. Byrne, L. Zhang, N. Anderson, K. Arumuganathan, and R. E. Ballard.2001. Two genetic linkage maps of tetraploid roses. Theor. Appl. Genet. 103:575–583.

Rehder, A. 1947. Manual of cultivated trees and shrubs hardy in North America. 2nd ed.Macmillan, New York.

Salesses, G., and A. Mouras. 1977. Tentative d’utilisation des protoplastes pour l’étude deschromosomes chez les Prunus. Ann. Amelior. Plantes 27:363–368.

Sargent, D. J., A. M. Hadonou, and D. W. Simpson. 2003. Development and characteriza-tion of polymorphic microsatellite markers from Fragaria viridis, a wild diploid straw-berry. Molec. Ecol. Notes 3:550–552.

Sargent, D. J., T. M. Davis, K. R. Tobutt, M. J. Wilkinson, N. H. Battey, and D. W. Simp-son. 2004. A genetic linkage map of microsatellite, gene specific and morphologicalmarkers in diploid Fragaria. Theor Appl. Genet. 109:1385–1391.

Sax, K. 1931. The origins and relationships of the Pomoideae. J. Arnold Arbor. 12:3–22.Sax, K. 1932. Chromosome relationships in the Pomoideae. J. Arnold Arbor. 13:363–367.Scorza, R., and W. B. Sherman. 1996. Peaches. p. 325–440. In: J. Janick and N. J. Moore

(eds.), Fruit breeding, Vol. I: Tree and tropical fruits. Wiley, New York.Seglias, N. P., and C. Gessler. 1997. Genetics of apple powdery mildew resistance from

Malus zumi (Pl2). Integrated control of pome fruit diseases. IOBC/WPRS Bulletin20:195–208.

Stam, P. 1993. Construction of integrated genetic linkage maps by means of a new com-puter package: JoinMap. Plant J. 3:739–744.

Stockinger, E. J., C. A. Mulinix, C. M. Long, T. S. Brettin, and A. F. Iezzoni. 1996. A link-age map of sweet cherry based on RAPD analysis of a microspore-derived callus cul-ture populations. J. Hered. 87:214–218.

Tanksley, S. D. 1983. Gene mapping. p. 109–138. In: S. D. Tanksley and T. J. Orton (eds.),Isozymes in plant genetics and breeding. Elsevier Science Publishers B.V., Amsterdam.

Tanksley, S. D., M. W. Ganal, J. P. Prince, M. C. de Vicente, M. W. Bonierbale, P. Broun,T. M. Fulton, J. J. Giovannoni, S. Grandillo, G. B. Martin, R. Messeguer, J. C. Miller, L.Miller, A. H. Paterson, O. Pineda, M. S. Röder, R. A. Wing, W. Wu, and N. D. Young.1992. High density molecular linkage maps of the tomato and potato genomes. Genet-ics 132:1141–1160.

Testolin, R. 2003. Marker assisted selection in stone fruits. Acta Hort. 622:163–176.van Ooijen, J. W., and R. E. Voorrips. 2002. JoinMap 3.0, software for the calculation of

genetic linkage maps. Plant Research International, Wageningen, The Netherlands.Vilanova, S., C. Romero, A. G. Abbott, G. Llácer, and M. L. Badenes. 2003a. An apricot

(Prunus armeniaca L.) F2 progeny linkage map based on SSR and AFLP markers, map-ping plum pox virus resistance and self-incompatibility traits. Theor. Appl. Genet.107:239–247.

Vilanova, S., C. Romero, D. Abernathy, A. G. Abbott, L. Burgos, G. Llacer, and M. L.Badenes. 2003b. Construction and application of a bacterial artificial chromosome(BAC) library of Prunus armeniaca L. for the identification of clones linked to the self-incompatibility locus. Molec. Genet. Genomics 269:685–691.

Vinatzer, B. A., H. B. Zhang, and S. Sansavini. 1998. Construction and characterization ofa bacterial artificial chromosome library of apple. Theor. Appl. Genet. 97:1183–1190.


04_4453.qxd 10/20/05 3:06 PM Page 210

Viruel, M., R. Messeguer, M. C. de Vicente, J. Garcia-Mas, P. Puigdomènech, F. Vargas, andP. Arús. 1995. A molecular marker map with RFLPs and isozymes for almond. Theor.Appl. Genet. 91:964–971.

Vision, T. J., D. G. Brown, and S. D. Tanksley. 2000. The origins of genomic duplicationsin Arabidopsis. Science 290:2114–2117.

Vowden, C. J., M. S. Ridout, and K. R. Tobutt. 1995. LINKEM: a program for genetic link-age analysis. J. Hered. 86:249–250.

Wang, D., R. Karle, T. S. Brettin, and A. F. Iezzoni. 1998. Genetic linkage map in sourcherry using RFLP markers. Theor. Appl. Genet. 97:1217–1224.

Weber, C. 1964. The genus Chaenomeles (Rosaceae). J. Arnold Arbor. 45:161–205.Weber, J. L., and P. E. May. 1989. Abundant class of human DNA polymorphism which

can be typed using the polymerase chain reaction. Am. J. Hum. Genet. 44:388–396.Westwood, M. N. 1978. Temperate-zone pomology. W. H. Freeman and Company, San

Francisco. p. 41–76.Wu, K. K., W. Burnquist, M. E. Sorrells, T. L. Tew, P. H. Moore, and S. D. Tanksley. 1992.

The detection and estimation of linkage on polyploids using single-dose restriction frag-ments. Theor. Appl. Genet. 83:294–300.

Xu, M. L., S. S. Korban, J. Q. Song, and J. M. Jiang. 2002. Constructing a bacterial artificialchromosome library of the apple cultivar Goldrush. Acta Hort. 595:103–112.

Yamamoto, T., T. Shimada, T. Imai, H. Yaegaki, T. Haji, N. Matsuta, M. Yamaguchi, andT. Hayashi. 2001a. Characterization of morphological traits based on a genetic linkagemap in peach. Breed. Sci. 51:271–278.

Yamamoto, T., T. Kimura, Y. Sawamura, K. Kotobuki, Y. Ban, T. Hayashi, and N. Matsuta.2001b. SSRs isolated from apple can identify polymorphism and genetic diversity inpear. Theor. Appl. Genet. 102:865–870.

Yamamoto, T., T. Kimura, M. Shoda, T. Imai, T. Saito, Y. Sawamura, K. Kotobuki, T.Hayashi, and N. Matsuta. 2002. Genetic linkage maps constructed by using an inter-specific cross between Japanese and European pears. Theor. Appl. Genet. 106:9–18.

Yamamoto, T., T. Kimura, T. Saito, K. Kotobuki, N. Matsuta, R. Liebhard, C. Gessler, W.E. van de Weg, and T. Hayashi. 2004a. Genetic linkage maps of Japanese and Europeanpears aligned to the apple consensus map. Acta Hort. 663(1):51–56.

Yamamoto, T., T. Kimura, J. Soejima, T. Sanada, Y. Ban, and T. Hayashi. 2004b. Identifi-cation of quince varieties using SSR markers developed from pear and apple. Breed. Sci.54:239–244.


04_4453.qxd 10/20/05 3:06 PM Page 211

Documents

Plant Breeding Reviews (Janick/Plant Breeding Reviews, Volume 27) || Synteny in the Rosaceae