The potassium transporter SlHAK10 is involved in ...€¦ · 13/02/2019 · 3 50 INTRODUCTION 51 Potassium (K+) is one of the three essential macronutrients, constituting 2-10% of

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Short title: SlHAK10 in Mycorrhizal Potassium Uptake 1

The potassium transporter SlHAK10 is involved in mycorrhizal 2

potassium uptake1 3

Jianjian Liu†a, Junli Liu†a, Jinhui Liua Miaomiao Cuia, Yujuan Huanga, Yuan Tiana, 4

Aiqun Chena,b,2,3, Guohua Xua,b,3 5

aState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and 6

Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China 7

bMOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze 8

River, Nanjing Agricultural University, Nanjing 210095, China. 9

†These authors contributed equally to this article 10

1 This work was supported by grants from the National Natural Science Foundation of China 11

(31572188, 31372121 and 31272225), and the Fundamental Research Funds for the Central Universities 12

(KYZ201868). This work was also supported by Graduate Student Scientific Research and Innovation 13

Projects in Jiangsu province (KYZZ16_0379), Jiangsu Collaborative Innovation Center for Solid 14

Organic Waste Resource Utilization, and the Innovative Research Team Development Plan of the 15

Ministry of Education of China (IRT1256). 16

2 Contacting author: [email protected] 17

The author responsible for distribution of materials integral to the findings presented in this 18

article in accordance with the policy described in the Instructions for Authors 19

(www.plantphysiol.org) is: Aiqun Chen ([email protected]). 20

3 Senior author. 21

One-sentence summary The gene SlHAK10 encodes a mycorrhiza-specific potassium transporter of 22

the KT/KUP/HAK family that mediates K+ uptake at the intraradical symbiotic interface in tomato. 23

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Plant Physiology Preview. Published on February 13, 2019, as DOI:10.1104/pp.18.01533

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Author contributions 25

J.J.L, A.Q.C, and G.H.X planned and designed the research; J.J.L, J.L.L, M.M.C and J.H.L performed 26

the experiments; J.J.L, Y.J.H and Y.T analyzed the data; J.J.L and A.Q.C wrote the manuscript. 27

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29

ABSTRACT 30

Most terrestrial plants form a root symbiosis with arbuscular mycorrhizal (AM) fungi, which receive 31

fixed carbon from the plant and enhance the plant’s uptake of mineral nutrients. AM symbiosis 32

improves the phosphorous and nitrogen nutrition of host plants; however, little is known about the 33

role of AM symbiosis in potassium (K+) nutrition. Here, we report that inoculation with the AM 34

fungus Rhizophagus irregularis improved tomato (Solanum lycopersicum) plant growth and K+ 35

acquisition, and K+ deficiency has a negative effect on root growth and AM colonization. Based on its 36

homology to a Lotus japonicus AM-induced K+ transporter, we identified a mycorrhiza-specific tomato 37

K+ transporter, SlHAK10 (Solanum lycopersicum High-affinity Potassium Transporter 10), that was 38

exclusively expressed in arbuscule-containing cells. SlHAK10 could restore a yeast K+ uptake-defective 39

mutant in the low-affinity concentration range. Loss of function of SlHAK10 led to a significant 40

decrease in mycorrhizal K+ uptake and AM colonization rate under low K+ conditions, but did not 41

affect arbuscule development. Overexpressing SlHAK10 from the constitutive CaMV35S promoter or 42

the AM-specific pSmPT4 promoter (Solanum melongena Phosphate Transporter 4) not only improved 43

plant growth and K+ uptake, but also increased AM colonization efficiency and soluble sugar content 44

in roots supplied with low K+. Our results indicate that tomato plants have a SlHAK10-mediated 45

mycorrhizal K+ uptake pathway and that improved plant K+ nutrition could increase carbohydrate 46

accumulation in roots, which facilitates AM fungal colonization. 47

48

Key words: Potassium uptake, Transporter, SlHAK10, Mycorrhiza, Symbiosis 49



3

INTRODUCTION 50

Potassium (K+) is one of the three essential macronutrients, constituting 2-10% of plant dry matter 51

(Leigh and Wyn Jones, 1984; Amrutha et al., 2007; Yang et al., 2009). As the most abundant cation in 52

living plant cells, K+ plays crucial roles in many fundamental processes, including photosynthesis, 53

osmoregulation, membrane transport, enzyme activation, and anion neutralization, and consequently 54

affects overall plant growth and development (Amrutha et al., 2007; Yang et al., 2009). As a result of 55

leaching losses, chemical fixation, and relatively low diffusion rate in soil, the availability of K+ 56

drastically fluctuates in large areas of agricultural land worldwide, and is often a limiting factor for 57

crop quality and yields (Rengel et al., 2008). 58

Plant cells need to maintain their cytoplasmic K+ concentrations at approximately 100 mM range 59

(Leigh and Wyn Jones, 1984; Walker et al., 1996), but the K+ concentration in the rhizosphere varies 60

drastically and rarely exceeds 0.01 to 1 mM (Maathuis et al., 2009; White, 2013). This indicates the 61

requirement for specialized transport systems for the uptake of K+ and for its internal redistribution 62

within plants. Transport of K+ through plant membranes can be mediated either by K+ channels, 63

which use the membrane potential and electrochemical gradient to facilitate K+ transport, or by 64

secondary transporters with different affinities located in the plasma or organelle membranes (Gierth 65

et al., 2005; Voelker et al., 2006; Li et al., 2017). Genes encoding plant K+ transporters are classified into 66

four major families: KT/HAK/KUP (K+ Transporter/High-affinity K+ transporter/K Uptake Permease), HKT 67

(High-affinity K+/Na+ Transporter), KEA (K+ Exchange Antiporters), and CHX (Cation/H+ Exchanger) (Cellier 68

et al., 2004; Kunz et al., 2014; Aranda-Sicilia et al., 2016; Wang et al., 2017). The KT/KUP/HAK family 69

comprises most of the plant K+ transporters identified so far, and members of this family are further 70

divided into four major clusters (I-IV) (Rubio et al., 2000; Grabov et al., 2007; Gupta et al., 2008; Wang et 71

al., 2013; Nieves-Cordones et al., 2016). Multiple transporters in cluster I, such as AtHAK5, HvHAK1, 72

OsHAK1, and OsHAK5, have high-affinity K+ uptake capacity and rapid up-regulation in response to 73

K+ deficiency (Schachtman et al., 1994; Santa-María et al., 1997; Gierth et al., 2005; Yang et al., 2014; 74



4

Chen et al., 2015). The cluster II members of the KT/KUP/HAK family showed great divergence in 75

sequence and function (Elumalai et al., 2002; Yang et al., 2009; Osakabe et al., 2013). Transporters in this 76

cluster have been characterized to mediate both high- and low-affinity K+ uptake. AtKUP1 from 77

Arabidopsis (Arabidopsis thaliana) is a typical cluster II member of the KT/KUP/HAK family that 78

functions as a dual-affinity K+ transporter (Fu et al., 1998). Much less has been reported regarding the 79

potential functions or physiological roles of the cluster III and IV transporters (Han et al., 2016). 80

Arbuscular mycorrhizal (AM) symbiosis, formed between AM fungi of Glomeromycotina and roots 81

of more than 80% of land plants, represents one of the most important symbiotic interactions in 82

nature (Smith et al., 2011). Formation of an AM symbiosis improves growth status for the plant 83

partner, especially under nutrient-poor growing conditions (Govindarajulu et al., 2005; Javot et al., 84

2007; Jin et al., 2012; Casieri et al., 2013; Courty et al., 2016; Garcia et al., 2016). In the nonmycorrhizal 85

plants, mineral nutrients can only be directly taken up from the rhizosphere via root epidermis and 86

root hairs. Once colonized by AM fungi, the mycorrhizal plants thus possess another indirect uptake 87

pathway, called the mycorrhizal pathway, via the AM fungal hyphae into root cortical cells (Sieh et al., 88

2012; Smith & Smith., 2012; Giovannetti et al., 2014). 89

The role of phosphate (Pi) nutrition in AM symbiosis has always been a major focus. It has been 90

repeatedly demonstrated that the mycorrhizal pathway is key for Pi uptake (Harrison et al., 2002; 91

Paszkowski et al., 2002; Nagy et al., 2006; Chen et al., 2007). Multiple plant transporters responsible for 92

transporting Pi across the intraradical symbiotic interfaces have been identified (Paszkowski et al., 93

2002; Yang et al., 2012; Xie et al., 2012; Chen et al., 2014). Although the contribution of AM fungi to the 94

transport of other nutrients is less clear, increasing evidence has shown that plants can acquire 95

substantial amounts of nitrogen (N) and sulfur (S), through the symbiotic uptake pathway (Mäder et 96

al., 2000; Allen et al., 2009; Giovannetti et al., 2014). 97

Compared with the relatively large number of reports on symbiotic P and N uptake, much less is 98

known about the effects of AM symbiosis on plant K+ acquisition. Nonetheless, enrichment of K+ in 99



5

different tissues of several mycorrhizal plants, including maize, Lactuca sativa, and wheat (Triticum 100

aestivum), could be traced in a small number of studies (Garcia and Zimmermann, 2014), leading to a 101

speculation that plants may also have a symbiotic K+ uptake pathway. This hypothesis gained some 102

support from the transcriptome analysis of both AM partners. On the fungal side, four sequences 103

from an EST library of R. irregularis were identified as K+ transporters (Casieri et al., 2013). On the 104

plant side, a KT/KUP/HAK transporter (Lj4g3v3116360.1, hereafter referred to as LjHAK) was shown 105

to be up-regulated in AM roots of Lotus japonicus compared with the nonmycorrhizal roots (Guether 106

et al., 2009). A recent study using whole-genome RNA sequencing of Medicago mycorrhizal roots 107

under K+ deficiency revealed the up-regulation of several genes encoding putative transporters, 108

including a putative K+/H+ exchanger, in mycorrhizal plants under K+ deprivation (Garcia et al., 2017). 109

However, in several transcriptome studies, no K+ transporter was observed to be up-regulated in M. 110

truncatula mycorrhizal roots (Gomez et al., 2009; Gaude et al., 2012). Thus, it is tempting to investigate 111

whether the gene regulation involved in the transfer of K+ from the AM fungus to the plant is 112

conserved across different plant species. 113

In this study, we performed extensive searches of putative K+ transporters in the recently released 114

transcriptomes for several mycorrhizal plants (Güimil et al., 2005; Fiorilli et al., 2009; Gomez et al., 2009; 115

Gaude et al., 2012; Garcia et al., 2017; Sugimura and Saito, 2017), which resulted in the identification of 116

a member of the KT/KUP/HAK family from tomato named SlHAK10 (Solyc03g097860.1.1) as the 117

putative orthologue of the AM-induced LjHAK. SlHAK10 was shown to be induced 500-fold in AM 118

roots compared with the nonmycorrhizal roots (Sugimura and Saito, 2017). Except LjHAK and 119

SlHAK10, none of the other K+ transporters from the KT/KUP/HAK family or other families showed 120

observable upregulation in the transcriptomes of tomato and Lotus japonicus mycorrhizal roots. 121

Genome-wide hunting and expression analysis of all the tomato KT/KUP/HAK genes confirmed that 122

SlHAK10 was the sole one having AM-inducible expression in this family. Tissue-specific and 123

functional analysis revealed that SlHAK10 was expressed exclusively in the cells containing 124



6

arbuscules and could mediate K+ uptake through the mycorrhizal pathway. These findings thus 125

indicate that there might be a mycorrhizal K+ uptake pathway in mycorrhizal plants, at least in tomato, 126

through activating the AM-induced K+ transporter(s), such as SlHAK10 and its potential orthologues. 127

128

129



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Results 130

AM symbiosis improves the K+ accumulation in tomato plants 131

In this study, to investigate the potential roles of AM formation in plant K+ acquisition, tomato plants 132

were grown in a sand-based pot culture in the presence or absence of AM fungus (R. irregularis) 133

supplied with 2 mM K+ as a high-K+ condition and with 0.2 mM K+ as a low-K+ condition. The plant 134

samples were harvested at 5 weeks postinoculation (wpi) for determining the shoot and root biomass, 135

K+ accumulation, and fungal colonization rates. 136

The plants treated with low-K+ solution showed a significant growth suppression in both shoots 137

and roots than the plants supplied with high K+ (Fig. 1a, b). Under low K+, root growth was more 138

inhibited compared with shoot growth, leading to a typical decrease in root:shoot ratio (Supplemental 139

Fig. S1a). Compared to the nonmycorrhizal (NM) plants, the mycorrhizal plants (AM plants) showed 140

increased shoot and root biomass under the high-K+ condition (Fig. 1a, b). The shoot K+ content in AM 141

plants grown under high K+ did not differ significantly with that in the NM plants (Supplemental Fig. 142

S1b), but the root K+ content (Supplemental Fig. S1c) and the total K+ accumulation in both shoots and 143

roots (Fig. 1c, d) increased by more than 20% in the AM plants. The shoot biomass of AM plants 144

supplied with low K+ had no significant difference compared with that of the NM control plants (Fig. 145

1a). By contrast, a significant increase in root biomass (Fig. 1b) and root:shoot ratio (Supplemental Fig. 146

S1), as well as K+ accumulation in both shoots and roots (Fig. 1c, d), could be observed under the 147

low-K+ condition. 148

The plants supplied with low K+ had a significantly lower AM colonization rate and arbuscule 149

incidence compared with the plants grown under high K+ (Fig. 1e, f). An assessment of 150

mycorrhization efficiency by different concentrations of K+ application was performed, which led to 151

the suggestion that K+-limiting growth condition might have a negative effect on AM colonization in 152

tomato (Supplemental Fig. S2). 153

Identification and characterization of a tomato AM-induced potassium transporter 154



8

A previous study based on microarray analysis revealed a putative AM-induced K+ transporter gene 155

(Lj4g3v3116360.1) of the KT/KUP/HAK family in Lotus japonicus (named LjHAK in this study) 156

(Guether et al., 2009). To identify the potential homologues responsive to AM symbiosis in tomato, the 157

coding sequence of LjHAK was employed for BLAST search against the tomato genomic database 158



9

(http://solgenomics.net/), which led to the identification of 21 nonallelic sequences with substantial 159

identities and similar structures as the tomato K+ transporter genes (Supplemental Fig. S3). 160

A phylogenetic tree constructed with these putative tomato K+ transporters (named SlHAK1 to 20 161

in this study) and homologues from several other plant species revealed a cluster of eight SlHAK 162

transporters with the AM-induced LjHAK in Group II of the KT/KUP/HAK family. Reverse 163

transcription quantitative PCR (RT-qPCR) analysis revealed that, with the exception of SlHAK10, the 164

closest orthologue of LjHAK, which was highly induced in the tomato mycorrhizal roots, none of the 165

other SlHAK genes showed significantly up-regulated response to AM symbiosis (Supplemental Fig. 166

S4). The mycorrhiza-inducible expression property of SlHAK10 was further confirmed by a recent 167

study on comparative transcriptome analysis between Lotus japonicus and tomato, in which SlHAK10 168

was shown to be induced 500-fold in AM roots (Sugimura and Saito, 2017). A time-course expression 169

analysis further proved the high correlation between the transcript abundance of SlHAK10 and 170

colonization intensity (Fig. 2a, b). The transcripts of SlHAK10 were barely detectable in other tissues, 171

including leaf, flower, and fruits, and showed no conspicuous induction to other environmental 172

factors, such as K+ and Pi deficiency, as well as high-Na+ stress (Supplemental Fig. S5). 173

To investigate the SlHAK10 expression pattern in detail, a 2281-bp promoter fragment of SlHAK10 174

was fused to the β-glucuronidase (GUS) reporter gene and introduced into tomato plants. The 175

resulting transgenic plants were then inoculated with R. irregularis. Five weeks after inoculation, the 176

GUS activity could be detected only in the mycorrhizal roots. Colocalization of GUS expression and 177

AM fungal structure by overlay of Magenta-GUS with trypan blue staining revealed that GUS activity 178

driven by the SlHAK10 promoter was confined to distinct cells containing arbuscules (Fig. 2c, d). No 179

GUS staining could be observed in the neighboring noncolonized cells, consistent with the results 180

reported for some other AM-specific nutrient transporters, such as Pi and NH4+ (Chen et al., 2011; 181

Kobae et al., 2010). 182



10

To determine whether SlHAK10 functions as a membrane-localized protein, its subcellular 183

localization was investigated. The coding sequence of SlHAK10 was fused in-frame with the 5’ end of 184

the eGFP reporter gene under the control of the 2×CaMV 35S promoter (2×35S::SlHAK10::eGFP). The 185

construct 35S::eGFP was used as a control. Both constructs were transiently expressed in the tobacco 186

(Nicotiana benthamiana) leaf epidermal cells via Agrobacterium tumefaciens-mediated infiltration. 187

Samples were stained using FM4-64FX, a plasma membrane-specific dye. Confocal microscopy 188

showed an overlap signal (yellow) of the GFP fluorescence (green) and FM4-64FX fluorescence (red) 189



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in the cells expressing the 2×35S::SlHAK10::eGFP chimeric gene (Fig. 3b), indicating that AM-specific 190

SlHAK10 might encode a plasma membrane-localized K+ transporter. 191

Functional characterization of SlHAK10 in yeast 192

The K+ transport capacity of SlHAK10 was initially evaluated by determining its ability to 193

complement a yeast mutant. Full-length SlHAK10 was introduced into the auxotrophic yeast mutant 194

strain R5421 (MATα ura3-52 leu2 trk1Δ his3Δ200 his4-15 trk2Δ1::pCK64). R5421 is defective in K+ 195

uptake and could not grow under low-K+ culture conditions. AtAKT1, a K+ channel from Arabidopsis, 196

was also transformed into R5421 as a positive control (Hirsch et al., 1998; Wang and Wu, 2013). The 197

yeast growth assays were carried out on AP medium containing different concentrations of K+. It was 198

shown that, under high-K+ conditions (5 and 10 mM), all the tested yeast strains could grow well, and 199

no visible difference was observed between the yeasts transformed with empty vector (pYES2) versus 200

the vector expressing SlHAK10. Along with the decline of K+ concentration from 5 to 1 mM, the 201



12

growth of R5421 harboring empty vector was almost entirely suppressed. Although the R5421 cells 202

transformed with SlHAK10 were also not able to grow at 0.5 mM K+, the yeast mutant expressing 203

SlHAK10 could indeed rescue its growth defect at 1 mM K+ (Fig. 4a). Growth kinetic analysis showed 204

that the yeast R5421 cells expressing AtAKT1 and SlHAK10 grew much faster than the yeast cells 205

harboring empty vector in liquid AP medium containing 1 mM KCl (Fig. 4b), suggesting that 206

SlHAK10 has K+ transport activity. 207

Loss-of-function mutation of SlHAK10 decreases mycorrhizal K+ uptake but does not affect 208

arbuscule morphology 209

As SlHAK10 is an AM-responsive K+ transporter in tomato, it is reasonable to speculate that SlHAK10 210

might have a contribution to the symbiotic K+ uptake and/or AM formation. To testify this hypothesis, 211

we first generated mutant lines of SlHAK10 by the CRISPR-Cas9 system. Two independent 212

homozygous mutant lines with one nucleotide deletion and insertion, respectively, in the coding 213

sequence of SlHAK10 were identified (Supplemental Fig. S6). The two mutant lines and wild-type 214



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(WT) plants were cultivated in a compartmented culture system containing a middle root/fungal 215

compartment (RFC) and two hyphal compartments (HCs) (Supplemental Fig. S7a). The RFC and HC 216

were separated by 30-μm nylon mesh. All three compartments were filled with a 4:1 mixture of 217



14

sterilized sand and low-K+ soil (the soil contains 30.2 mg kg-1 available K and 18.5 mg kg-1 available P). 218

Two plants (mutant or WT) were grown in the RFC in the presence or absence of R. irregularis for 5 219

weeks. All the plants were watered weekly with nutrient solution containing either 2 mM K+ as a 220

high-K+ condition or 0.2 mM K+ as a low-K+ condition. To monitor whether fungal hyphae could reach 221

and take up nutrients from HCs, additional 15N-labled Ca(NO3)2 was introduced into the two HCs by 222

watering. Compared to the inoculated WT and mutant plants, 15N accumulation in all the 223

noninoculated plants was extremely low (Supplemental Fig. S7b), suggesting that fungal hyphae can 224

absorb nutrients from HCs and almost no ion diffusion across the nylon meshes occurred. In all the 225

treatments, the mutant plants showed a comparable total biomass with the WT plants (Fig. 5a, b). No 226

significant difference in the K+ accumulation could be detected between the nonmycorrhizal WT and 227

mutant plants grown under both the K+ supply conditions (Fig. 5c-f), while the K+ contents decreased 228

by nearly 20% in both shoots and roots of the mycorrhizal mutant plants compared to those in the 229

mycorrhizal WT plants (Fig. 5d, f). As it is well established that AM fungal colonization has a 230

dominant contribution to plant P nutrition, the P contents in these plants was also determined. As 231

expected, all the inoculated WT and mutant plants contained significantly higher P in both shoots and 232

roots than those in the nonmycorrhizal plants (Supplemental Fig. S8a-d). The P contents in 233

mycorrhizal mutant plants grown under low K+ were significantly decreased compared to those in the 234

mycorrhizal WT plants (Supplemental Fig. S8b, d). The mycorrhizal mutant plants also contained a 235

significantly lower P in their roots than the mycorrhizal WT plants grown under high K+ 236

(Supplemental Fig. S8c). 237

To determine whether SlHAK10 might be involved in the regulation of AM symbiosis, the degree of 238

AM colonization in the mycorrhizal roots of WT and mutant lines was assessed. Compared to WT 239

plants, both the total colonization rate and arbuscule abundance were significantly reduced in the 240

mutant lines grown under the low K+ supply condition (Fig. 6a, b), while the arbuscule morphology in 241

the mutant lines was not significantly impaired (Fig. 6c, d). These findings suggest that SlHAK10 is 242



15

involved in mycorrhizal K+ uptake but is not essential for arbuscule development. Several recent 243

studies have pointed to an important role of the host-derived fatty acids in maintaining AM 244

symbiosis. The assay of fatty acid contents in the mycorrhizal roots of WT and slhak10 mutant plants 245

showed no significant difference under both the K+ supply conditions (Supplemental Fig. S9). A 246

further investigation of the soluble sugar content revealed that in the absence of AM fungal 247

colonization, both the WT and slhak10 mutants supplied with low K+ contained significantly higher 248

soluble sugar in their shoots, but a lower amount in their roots, compared to plants grown under high 249

K+ (Fig. 7a-d). The soluble sugar content in the mycorrhizal roots of mutant plants was significantly 250

lower than those in the WT mycorrhizal roots under the low-K+ supply condition (Fig. 7c-d). 251



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Overexpressing SlHAK10 improves K+ uptake and mycorrhizal colonization under K+ deficiency 252

conditions 253

To assess whether overexpression of SlHAK10 can facilitate K+ uptake, we further generated 254

transgenic tomato plants overexpressing SlHAK10 under either the constitutive Cauliflower mosaic 255

virus 35S promoter (CaMV35S) or the AM-specific promoter pSmPT4. We have previously proven 256

that pSmPT4, the promoter of an eggplant (Solanum melongena) Pi transporter, could drive GUS 257

reporter expression exclusively in AM fungal-colonized cells (Chen et al., 2007; Chen et al., 2011). 258

RT-qPCR analysis showed that the expression of SlHAK10 was greatly increased in the mycorrhizal 259



17

roots of the overexpression (OE) lines (Supplemental Fig. S10). Four independent transgenic lines 260

(35S-OE2 and 35S-OE6, overexpression driven by the CaMV35S promoter; pSmPT4-OE1 and 261

pSmPT4-OE4, overexpression driven by the pSmPT4 promoter) were thus selected for analysis of K+ 262



18

absorption in sand-based pot culture inoculated with R. irregularis for 5 weeks. All the plants were 263

irrigated with nutrient solution containing either 2 mM K+ as a high-K+ condition or 0.2 mM K+ as a 264

low-K+ condition. In the presence of AM colonization, overexpressing SlHAK10 could significantly 265

increase the biomass of plants grown under the low-K+ condition (Fig. 8a, b). Compared to WT plants, 266

all the 35S-OE lines showed a significantly higher K+ accumulation in both shoots and roots under 267

both K+ supply conditions, irrespective of the presence or absence of AM inoculation (Fig. 8c-f). It is 268

worth noting that the nonmycorrhizal 35S-OE plants showed a comparable K content in both shoots 269

and roots as the mycorrhizal 35S-OE plants, suggesting that constitutive overexpression of SlHAK10 270

may mask the contribution of mycorrhizal K uptake pathway mediated by the native SlHAK10. This 271

speculation seems to be reasonable, as the transcripts of SlHAK10 were increased nearly 100-fold in 272

the mycorrhizal roots of 35S-OE lines (Supplemental Fig. S10). With respect to the pSmPT4-OE lines, 273

increased K+ uptake, as indicated by significantly higher shoot and root K+ contents compared with 274

the WT plants, could be detected only in the mycorrhizal plants. As expected, no significant 275

difference in either plant biomass or K+ content could be detected between the nonmycorrhizal WT 276

and pSmPT4-OE plants grown under both the K+ conditions (Fig. 8). 277

The WT plants grown under low K+ conditions showed a significant decrease in AM colonization 278

compared with the plants grown under the high K+ conditions (Fig. 9). Overexpressing SlHAK10 from 279

either promoter significantly improved the total fungal colonization and arbuscule abundance under 280

the low-K+ condition. Consistent with this, the P contents in the mycorrhizal overexpressing lines 281

grown under low K+ were also significantly increased compared with the WT plants (Supplemental 282

Fig. S11). The increased mycorrhizal colonization in the roots of SlHAK10-OE plants could also be 283

seen in the increased expression of SlPT4 (SlPT4) and RiTub (Fig. 9c, d), the two marker genes used 284

for evaluating AM colonization (Liao et al., 2015; Floss et al., 2013). A further assay of the soluble sugar 285

contents showed that the SlHAK10-OE plants grown under low K+ contained significantly higher 286

soluble sugar contents in their mycorrhizal roots compared to the WT plants (Fig. 10). 287



19

288

289



20

Discussion 290

Contributing effects of AM fungal colonization on tomato plant growth and K+ acquisition 291

Improving availability of mineral nutrients for plants is one of the major contributions of AM 292

symbiosis. Although the role of AM symbiosis in plant K+ nutrition received much less attention than 293

P and N (Mäder et al., 2000; Nagy et al., 2006; Chen et al., 2007; Javot et al., 2007), an increased K 294

accumulation in distinct tissues upon AM symbiosis has been reported related to diverse plant 295

species (Perner et al., 2007; Baslam et al., 2013; Oliveira et al., 2016). Physiological analysis of the 296

AM-associated responses of Medicago truncatula plants revealed a significant increase of root biomass 297

and K+ content in AM plants under the K+ deprivation condition (Garcia et al., 2017). In this study, we 298



21

also observed that the AM tomato plants had a higher root biomass by more than 20% than the NM 299

plants under the low-K+ condition (Fig. 1b). However, in the high-K+ treatment, the AM plants showed 300

more growth advantages, with shoot and root biomass increased by nearly 40% compared with the 301

NM control plants (Fig. 1a, b). Moreover, inoculation with AM fungus resulted in a much higher K+ 302

accumulation in AM plants than the NM plants, irrespective of K+ regimen (Fig. 1c, d). These findings 303

highlighted the positive roles of AM fungal colonization in tomato plant growth and K+ acquisition. 304

However, it could not be ruled out that the increased K+ accumulation in mycorrhizal tomato plants 305

might be a partial consequence of an improved P uptake, as earlier studies have proposed K+ to be 306

one of the major counter-ions of polyphosphates, which forms a phosphate reserve for the host plant 307

in AM symbiosis (Bücking and Heyser, 1999). A recent study of K nutrition of ectomycorrhizal Pinus 308

pinaster showed that altered K+ transfer towards the host plant could affect fungal P translocation to 309

the shoots, suggesting that interactions would also take place during the uptake of K+ and Pi by 310

ectomycorrhizal plants (Garcia et al., 2014). 311

SlHAK10 is involved in the mycorrhizal K+ uptake at the intraradical symbiotic interface 312

The increased K+ accumulation in mycorrhizal tomato plants is a strong hint of the presence of an AM 313

symbiotic pathway for K+ uptake in tomato. SlHAK10, the AM-induced K+ transporter, was proposed 314

to be the suitable candidate for K+ uptake at the symbiotic interface, as its expression was specifically 315

confined in the cells containing arbuscules (Fig. 2). Its capacity in K+ transport was demonstrated in 316

both the heterologous yeast system and transgenic plants. Overexpression of SlHAK10 with the 317

constitutive CaMV35S promoter led to a significant increase of K+ uptake under both the high-K+ (2 318

mM) and low-K+ (0.2 mM) conditions, regardless of the presence or absence of AM fungal 319

colonization (Fig. 8). 320

The evidence for the action of SlHAK10 in mycorrhizal K+ uptake was obtained through analysis of 321

slhak10 mutants in the compartmented culture in the inoculation condition. Knockout of SlHAK10 322

significantly reduced the uptake of K+ from the HCs, resulting in lower K+ contents in both shoots and 323



22

roots of the slhak10 mutants, relative to the wild-type plants (Fig. 5). More indirect evidence was 324

obtained through the overexpression of SlHAK10 in tomato under the control of a strong, AM-specific 325

promoter, pSmPT4. Overexpressing SlHAK10 exclusively in mycorrhizal roots resulted in a significant 326

increase of K+ content in both shoots and roots of the mycorrhizal transgenic plants compared to the 327

WT plants (Fig. 8). Interestingly, the 35S-OE mycorrhizal plants seemed to have a higher K+ content in 328

shoots than the pSmPT4-OE plants grown under low K+ (Fig. 8d). Such discrepancy in K+ 329

accumulation might be caused by different expression efficiency and tissue localization of SlHAK10 330

controlled by the two kinds of promoters. A previous study demonstrated that blocking mycorrhizal 331

Pi transport by silencing AM-induced Pi transporter MtPT4 in Medicago could severely impair 332

arbuscule formation (Javot et al. 2007). The absence of defective arbuscular morphology in the slhak10 333

mutants observed in this study (Fig. 5) suggests that transport of K+ across the symbiotic interface 334

might not be a requirement for arbuscule development. Even so, the identification of an orthologue of 335

SlHAK10 in Lotus japonicus that also showed an inducible response to AM symbiosis (Guether et al., 336

2009) is evidence that the regulatory mechanism regarding the AM-mediated K+ uptake pathway 337

might be conserved across different plant families. 338

Improving plant K+ nutrition may facilitate AM colonization under the K+ deficiency condition 339

The availability of mineral nutrients, in particular P, has a strong impact on AM colonization (Nagy et 340

al., 2009; Breuillin et al., 2010; Nouri et al., 2014; Johnson et al., 2015). P and N starvation was also 341

characterized as being able to induce a stress-responsive transcriptional reprogramming that is 342

beneficial for AM colonization (Bonneau et al., 2013). However, the effect of plant K+ nutrition on AM 343

colonization has not been well characterized thus far. A recent study regarding the mycorrhizal 344

Medicago plants showed that K+ availability did not affect the establishment of AM symbiosis (Garcia 345

et al., 2017). However, the conclusions derived from different symbiotic systems were not always 346

consistent, as in some other studies a positive effect on AM colonization by K+ application has been 347

proposed (Zhang et al., 2017). 348



23

In this study, we found that mycorrhizal tomato plants supplied with high K+ had a significantly 349

higher AM colonization rate and arbuscule incidence than the K+-deficient plants (Fig. 1f, 350

Supplemental Fig. S1). Previous studies have shown that in K+ starvation plants, the export of 351

carbohydrates from source leaves and the allocation to roots were heavily interrupted, leading to a 352

severe repression in root growth and a typical decrease in root:shoot ratio (Cakmak et al., 1994a,b; 353

Deeken et al., 2002; Hermans et al., 2006; Kanai et al., 2007; Pettigrew, 2008; Cai et al., 2012). In tomato, 354

it has been revealed that K+ deficiency caused a decreased sugar accumulation in roots (Kanai et al., 355

2007). In this study, we also observed a significant increase of soluble sugar contents in shoots but 356

decrease in roots of both WT and mutants grown under K+ deficiency (Fig. 7). Additionally, 357

overexpressing SlHAK10 by either the constitutive CaMV35S promoter or the AM-specific pSmPT4 358

promoter under K+ deficiency led to not only an improvement in K+ absorption, but also a significant 359

increase in AM colonization and soluble sugar accumulation in roots (Fig. 8, 9, 10). Considering that 360

maintenance of AM symbiosis requires the transfer of substantial amounts of plant-fixed 361

carbohydrates to AM fungi, it is reasonable to speculate that improving K+ uptake under K+ deficiency 362

may promote carbohydrate allocation to roots, which facilitates root growth and AM colonization. 363

Such a hypothesis could gain indirect support from an earlier study reporting that silencing a fungal 364

monosaccharide transporter, MST2, with a broad substrate spectrum, impaired mycorrhiza formation 365

in M. truncatula mycorrhizal roots (Helber et al., 2011). 366

In conclusion, in this study, we characterized the potential interactions between K+ nutrition and 367

AM symbiosis in tomato and assessed the function of a K+ transporter, SlHAK10, in both the 368

heterologous yeast system and transgenic plants. We demonstrated that there is a SlHAK10-mediated 369

mycorrhizal K+ uptake pathway in tomato and that improving plant K+ nutrition under the low-K+ 370

condition may increase carbohydrate accumulation in roots and facilitate AM fungal colonization. As 371

a mutually stimulating mechanism has been revealed to exist during the simultaneous exchange of C 372

and P/N between the AM partners, it would be interesting to investigate in the future whether the 373



24

“free-market” model is also applicable to the exchange of K and C during AM symbiosis. 374

375

Materials and methods 376

Plant materials and growth conditions 377

Tomato (Solanum lycopersicum L. cv MicroTom) plants were used in this study. Seeds of the wild-type 378

(WT) and transgenic plants were surface sterilized with 10% sodium hypochlorite for 10 min and then 379

germinated in a growth chamber programmed for 16-h light at 28 °C and 8-h dark at 20 °C. The 380

seedlings were then transplanted to sterilized quartz-sand for a 2-week culture irrigated with 381

full-strength nutrient solution containing the following: 1 mM NH4+, 4 mM NO3-, 2 mM K+, 1 mM Pi, 382

0.75 mM Ca2+, 0.5 mM Mg2+, 0.25 mM Cl−, 0.5 mM SO42−, 20 μM Fe2+, 9 μM Mn2+, 46 μM BO33−, 8 μM 383

Zn2+, 3 μM Cu2+, and 0.03 μM MoO42−. The plantlets were then transferred to either sand-based pot 384

culture or a compartmented culture system for inoculation with AM fungi. 385

For sand-based pot culture, three plantlets were transplanted to a 3 dm3 pot filled with sterilized 386

sand. A sand-based mycorrhizal inoculum containing Rhizophagus irregularis (previously named 387

Glomus intraradices) was used for colonization. Each plantlet was inoculated with 1.2 g of inoculum 388

containing approximately 200 spores around the roots. The nonmycorrhizal control plants were 389

obtained by inoculation with autoclaved inoculum. The plants were supplied with nutrient solution 390

including either 2 mM K+ as a high-K+ treatment or 0.2 mM K+ as a low-K+ treatment. To guarantee 391

high mycorrhizal colonization, the plants in pot culture were watered with a relatively low 392

concentration (50 μM) of Pi. 393

A compartmented culture system was employed to investigate the contribution of SlHAK10 to 394

mycorrhizal K uptake by using two loss-of-function slhak10 mutant lines. The culture system contains 395

a middle root/fungal compartment (RFC) and two hyphal compartments (HCs) (Fig. S7a). All three 396

compartments were filled with a 4:1 mixture of sand and soil (the soil contains 30.2 mg kg-1 available 397

K and 18.5 mg kg-1 available P). Two mutant lines or WT plants were grown in the RFC in the 398



25

presence or absence, respectively, of R. irregularis inoculation for 5 weeks. All the plants were watered 399

weekly with nutrient solution containing either 2 mM K+ as a high-K+ condition or 0.2 mM K+ as a 400

low-K+ condition. To prevent ion diffusion between the RFC and HCs, the RFC was separated from 401

the HCs by two iron gauzes with a 0.5-cm air gap. A 30-μm nylon mesh was placed between the two 402

iron gauzes to prevent roots from entering the HCs. To monitor whether fungal hyphae could reach 403

and take up nutrients from HCs, additional 15N-labeled Ca(NO3)2 was introduced into the two HCs by 404

watering, and 15N accumulation in the mycorrhizal plants and nonmycorrhizal plants was 405

determined. 406

RT-qPCR 407

For performing RT-qPCR analysis, approximately 2 μg of total RNA from each sample was used to 408

synthesize cDNA using a reverse transcription kit (TAKARA), and the synthesized cDNAs were used 409

as templates for the following RT-qPCR analysis. The PCR was conducted on an Applied Biosystems 410

Plus Real-Time PCR System using the SYBER premix ExTaq kit (TAKARA). The specific primer pairs 411

for each of the HAK genes are listed in Supplementary Table S1. The relative transcript abundance of 412

each target gene was standardized to the transcript level of a tomato constitutive Actin gene (Chen et 413

al., 2014). 414

Identification of HAK genes in tomato 415

Members of the KT/KUP/HAK gene family in the tomato genome were identified using the BLASTN 416

and TBLASTN algorithms. To identify the potential HAK genes in the tomato genome, the coding 417

sequence of the AM-induced Lotus japonicus K+ transporter (Lj4g3v3116360.1) (Guether et al., 2009) 418

was employed for the BLAST search against the tomato genomic sequence database 419

(www.sgn.cornell.edu). Sequences with a query over 50% and e-value less than -10 were taken as the 420

candidates. All obtained sequences were submitted to NCBI (http://www.ncbi.nlm.nih.gov/) for 421

further confirmative analysis. 422

Subcellular localization analysis 423



26

For subcellular localization analysis of SlHAK10 by agroinfiltration of tobacco leaves, the full-length 424

coding sequence (cds) of SlHAK10 without the stop codon was first ligated to an intermediate vector, 425

pSAT6AEGFP-N1. The SlHAK10-GFP fusion construct as well as GFP alone were then subcloned into 426

the expression vector pRCS2-ocs-nptII with the rare restriction enzyme PI-PspI. The plasmids were 427

then transformed into the Agrobacterium tumefaciens strain EHA105. The bacterial cells were harvested 428

by centrifugation and resuspended in a solution (pH 5.7) containing 10 mM MES, 10 mM MgCl2, and 429

200 μM acetosyringone. Cell suspensions at an optical density (600 nm) of 0.1 were infiltrated into the 430

leaves of Nicotiana benthamiana using a needle-free syringe. Green fluorescent protein (GFP) 431

fluorescence in the transformed leaves was imaged using confocal microscopy (Leica Confocal 432

TCS-SP8) after 48-72 h. 433

Construction of binary vector and plant transformation 434

To construct the SlHAK10 promoter vector, a 2281-bp-long promoter fragment of SlHAK10 435

immediately upstream of the translation start ATG was amplified by PCR to introduce HindIII and 436

BamHI restriction sites at the end of the 5’ and 3’ regions, respectively. After digestion with the two 437

restriction enzymes, the amplified fragments were cloned into binary vector pBI121 to replace the 438

CaMV35S promoter in front of the GUS reporter gene. The generated vector was used for tomato 439

transformation by the EHA105 strain. 440

To construct the SlHAK10 constitutive overexpression vector, the coding sequence of SlHAK10 was 441

amplified and cloned into the binary vector pCAMBIA 1300 using the ClonExpress II One Step 442

Cloning Kit (Vazyme Biotech, Nanjing, China). The resulting construct (named 35S-SlHAK10) in 443

which SlHAK10 was controlled by the CaMV35S promoter was introduced into A. tumefaciens EHA105 444

strain for transformation of tomato and rice plants, respectively. To construct the SlHAK10 445

AM-specific overexpression vector, an 865-bp-long promoter fragment of the AM-specific Pi 446

transporter gene SmPT4 (Chen et al., 2011) was amplified and cloned into the 35S-SlHAK10 construct 447

to replace the CaMV35S promoter. The recombinant construct (named pSmPT4-SlHAK10) was also 448



27

introduced into the EHA105 strain for transformation of tomato plants. 449

The CRISPR/Cas9 gene knockout constructs were generated using the commercial vector VK005-03 450

(Viewsolid Biotech, Beijing, China). Two spacers were designed to target two different sites in exons 451

of SlHAK10. For site 1, we used the oligo pair 5’-TGGATCCTTGCCATATCAAATC-3’ and 452

5’-AACGATTTGATATGGCAAGGAT-3’; and for site 2, we used the oligos 5’- 453

TGGACAGACCTAAGTCCCGGACT-3’ and 5’-AACAGTCCGGGACTTAGGTCTGT-3’. The oligo 454

pairs were first annealed to produce a double-stranded fragment with 3-nt 5’ overhangs at both ends 455

and then ligated into the linearized vector VK005-03. 456

Agrobacterium-mediated transformation of tomato plants was performed according to the protocol 457

described by Sun et al. (2006). The transformation of rice plants was carried out as described 458

previously (Upadhyaya et al., 2000). 459

Functional characterization of SlHAK10 in yeast 460

The full-length coding sequences of SlHAK10 and AtAKT1 were inserted into yeast expression vector 461

p-YESII under the control of the Met promoter (Bernstein et al., 2013). The resulting vectors were 462

transformed into the yeast mutant strain R5421 (MATα ura3-52 leu2 trk1Δ his3Δ200 his4-15 463

trk2Δ1::pCK64), in which two endogenous K+ transporter genes (TRK1,2) were deleted (Li et al., 2014). 464

The yeast cell transformation was performed using the LiAC/ssDNA/PEG method, and the growth 465

assays on arginine phosphate (AP) medium were performed as described by Horie et al. (2011). 466

Determination of the concentrations of K, P, and soluble sugars 467

The dried plant material was digested with 98% H2SO4 and 30% hydrogen peroxide as described 468

previously (Chen et al., 2007). The K+ concentration in the solution was measured by an ICP emission 469

spectrometer (Optima 2100DV; PerkinElmer Inc., Shelton, CT, USA) as described by Cai et al. (2012). 470

The total P concentration was measured using the molybdate blue method as described previously 471

(Chen et al., 2007). The measurement of soluble sugar concentrations was conducted based on the 472

method of Hansen and Møller (1975), as described in detail by Chen et al. (2015). 473



28

Analysis of fatty acid contents 474

Extraction of fatty acid methyl esters (FAMEs) from tomato roots was performed using the modified 475

method of Browse et al. (1986) and Jiang et al. (2017). Briefly, 50 mg of root samples was finely ground 476

in liquid nitrogen and then transferred into 2-ml centrifugal tubes containing 1 ml 5% H2SO4 (v/v in 477

methanol). The samples were then heated to 80°C for 1 h. After cooling, extraction solution containing 478

30 μl of methyl nonadecanoate, 0.3 ml of hexane, and 1 ml of 0.9% NaCl was added to the samples 479

and then shaken vigorously for five minutes. After centrifugation, the hexane phase containing the 480

FAMEs was collected and used for determination by GC-MS (GC-FID, Agilent 7890A Plus GC; Agilent, 481

Santa Clara, CA, USA). The parameters for the GC-MS assay were used as described by Jiang et al. 482

(2017). 483

Detection of mycorrhizal colonization and Histochemical GUS staining 484

The examination of mycorrhizal fungal colonization was performed using the magnified line 485

intersection method (McGonigle et al., 1990). Root samples were cut randomly into 1-cm pieces and 486

cleared for 3 h at 70°C in 10% (w/v) KOH solution, and then the root segments were stained in 0.3% 487

trypan blue at 90°C for 2 h. Ten 1-cm root segments were mounted on a microscope slides, and each of 488

these segments was investigated at 10 randomly chosen spots, which were scored for the presence of 489

hyphae, arbuscule, vesicle, or none (absence of any fungal structures). For each root system, three to 490

four microscope slides were employed. The total colonization level (root length colonization%) was 491

calculated by the formula, number of intersections cutting through any fungal structures/total 492

number of intersections examined; and the arbuscular colonization level (arbuscule abundance%) was 493

calculated by the formula, number of intersections cutting through at least one arbuscule/total 494

number of intersections examined. At least three different root systems were evaluated for each 495

genotype. Histochemical staining of the GUS activity in transgenic plants was performed as described 496

previously (Karandashov et al., 2004). 497

498



29

Statistical analysis 499

The data were analyzed by ANOVA (SPSS 16.0; SPSS Inc., Chicago, IL, USA), followed by Tukey’s 500

test (P < 0.05), to test differences between different plant genotypes and treatments. The data 501

represent the mean ± SE of five independent biological replicates. 502

Accession Numbers 503

Sequence data from this article can be found in the aramemnon data libraries 504

(http://aramemnon.botanik.uni-koeln.de/) under accession numbers: SlHAK1 (Solyc08g015680), SlHAK2 505

(Solyc06g050170), SlHAK3 (Solyc12g096580), SlHAK4 (Solyc12g017910), SlHAK5 (Solyc12g005670), 506

SlHAK6 (Solyc02g087000), SlHAK7 (Solyc04g025880), SlHAK8 (Solyc05g005740), SlHAK9 507

(Solyc10g047270), SlHAK10 (Solyc03g097860), SlHAK11 (Solyc01g105150), SlHAK12 508




(Solyc09g074820). 512

513

Supplemental Data 514

Figure S1. Effects of different K+ applications and AM fungal colonization on root:shoot ratio and K+ 515

uptake. 516

Figure S2. Effects of different K+ applications on AM colonization. 517

Figure S3. Phylogenetic analysis and exon/intron organization of tomato HAK transporters. 518

Figure S4. Expression analysis of tomato HAK genes in response to AM symbiosis. 519

Figure S5. Tissue-specific expression analysis of SlHAK10. 520

Figure S6. Screening the homozygous mutant lines of SlHAK10 by PCR sequencing. 521



30

Figure S7. Effects of mutation of SlHAK10 on tomato growth under a compartmented culture condition. 522

Figure S8. Effects of mutation of SlHAK10 on mycorrhizal P uptake in tomato plants grown under a 523

compartmented culture condition. 524

Figure S9. The fatty acid contents in the mycorrhizal roots of WT and slhak10 mutant plants. 525

Figure S10. SlHAK10 is overexpressed in mycorrhizal roots of transgenic tomato plants. 526

Figure S11. Effects of overexpression of SlHAK10 on tomato P acquisition under a sand-based pot culture 527

condition. 528

Table S1. List of the primers used for RT-qPCR analysis in this study. 529

530

Acknowledgments 531

This research was funded by National Natural Science Foundation of China (31572188, 31372121 and 532

31272225) and the Fundamental Research Funds for the Central Universities (KYZ201868). This work 533

was also supported by Graduate Student Scientific Research and Innovation Projects in Jiangsu 534

province (KYZZ16_0379), Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource 535

Utilization, and the Innovative Research Team Development Plan of the Ministry of Education of 536

China (IRT1256). We thank Dr. Rick Gaber from Northwestern University for kindly providing the 537

yeast mutant R5421. 538

539

Legends of Figures 540

Figure 1. Impact of different K+ applications and AM fungal colonization on tomato plant 541

growth and K+ acquisition. (a, b) Shoot (a) and root (b) biomass of AM and NM plants. (c, d) 542

K+ accumulation in shoots (c) and roots (d) of AM and NM plants. (e, f) Total colonization 543

rate (e) and arbuscule abundance (f) under high-/low-K+ supply conditions. AM: AM 544



31

fungal-colonized plants; NM: nonmycorrhizal plants. Error bars indicate SE (n=5). The 545

asterisk indicates a significant difference (P < 0.05). 546

Figure 2. Expression analysis of SlHAK10 in response to AM symbiosis. (a) Quantification of 547

AM fungal colonization at different sampling time points. dpi, days postinoculation. (b) 548

Time-course expression of SlHAK10 in mycorrhizal roots of tomato plants. Values are the 549

means of three biological replicates with SEs. Different letters indicate a significant 550

difference (P<0.05). (c, d) Histochemical GUS staining of tomato roots expressing 551

pSlHAK10::GUS in the absence (c) and presence (d) of R. irregularis inoculation. Red arrows 552

indicate arbuscules. Blue arrows denote noncolonized cells in mycorrhizal roots. Scale bars 553

=50um. 554

Figure 3. Subcellular localization analysis of SlHAK10. Confocal laser scanning microscopy 555

images of tobacco (N. benthamiana) leaf epidermal cells transiently expressing 35S::eGFP (a) 556

or 35S::SlHAK10-GFP (b). (I) Confocal images under GFP channel only. (II) FM4-64FX 557

dye-induced red fluorescence showing the position of plasma membrane. (III) BF, bright 558

field. (IV) Merged images of GFP fluorescence (green) and FM4-64FX fluorescence (red). 559

Scale bars =50um. 560

Figure 4. Functional complementation of SlHAK10 for K+ acquisition in the K+ 561

uptake-defective yeast strain R5421. (a) Growth status of R5421 cells expressing AtAKT1, 562

empty vector (pYES2), and SlHAK10 on arginine phosphate (AP) medium supplemented 563

with 10, 5, 1, and 0.5 mM KCl. Each transformant was precultured in liquid AP medium 564

containing 100 mm KCl. The 1:10 serial dilutions of yeast cells were spotted on the AP 565

medium, and then incubated at 30°C for 6 d. (b) Growth kinetic analysis of the yeast R5421 566



32

cells expressing AtAKT1, empty vector, and SlHAK10 cultured in liquid AP medium 567

containing 1 mM KCl. Errors bars represent SDs of five biological replicates. The asterisk 568

indicates a significant difference (P < 0.05). 569

Figure 5. Effects of mutation of SlHAK10 on the total biomass and K+ accumulation in 570

tomato grown under a compartmented culture condition. All the compartments were filled 571

with a 4:1 mixture of sand and low-K+ soil (the soil contains 30.2 mg kg-1 available K and 18.5 572

mg kg-1 available P). Wild-type and mutant plants were grown in the RFC for AM fungal 573

inoculation. Plants were watered weekly with either high-K+ (2 mM K+) or low-K+ (0.2 mM K+) 574

solution. The total biomass (a, b) and K+ contents in shoots (c, e) and roots (d, f) of the 575

wild-type and mutant plants were determined at 5 weeks postinoculation (wpi). AM: 576

mycorrhizal plants; NM: nonmycorrhizal plants. Error bars indicate SEs (n=5). The asterisk 577

indicates a significant difference (P < 0.05). 578

Figure 6. Effects of mutation of SlHAK10 on the AM colonization and arbuscule morphology. 579

Wild-type and mutant plants were grown in a compartmented culture system. Plants were 580

watered weekly with either high-K+ (2 mM K+) or low-K+ (0.2 mM K+) solution. The total root 581

length colonization (a) and arbuscule abundance (b) in the mycorrhizal roots of wild-type 582

and mutant plants were assessed at 5 weeks postinoculation (wpi). Arbuscules stained with 583

WGA-AF-488 in the mycorrhizal roots of wild-type (c) and mutant plants (d). Error bars 584

indicate SEs (n=5). The asterisk indicates a significant difference (P < 0.05). 585

Figure 7. The contents of soluble sugar in the WT and slhak10 mutant plants. Wild-type and 586

mutant plants were grown in a compartmented culture system. Plants were watered weekly 587

with either high-K+ (2 mM K+) or low-K+ (0.2 mM K+) solution. The soluble sugar 588



33

concentrations in the shoots (a, b) and roots (c, d) of wild-type and mutant plants were 589

determined at 5 weeks postinoculation (wpi). AM: mycorrhizal plants; NM: nonmycorrhizal 590

plants. Error bars indicate SEs (n=5). The asterisk indicates a significant difference (P < 0.05). 591

Figure 8. Effects of overexpression of SlHAK10 on tomato growth and K+ acquisition under a 592

sand-based pot culture condition. 35S-OE, SlHAK10 was overexpressed under the control of 593

the constitutive CaMV35S promoter; pPT4-OE, SlHAK10 was overexpressed under the 594

control of a mycorrhiza-specific Pi transporter promoter pSmPT4. Two-week-old seedlings 595

were grown in sand-based pot culture for AM fungal inoculation for 5 weeks. The plants 596

were treated with either high-K+ (2 mM K+) or low-K+ (0.2 mM K+) solution. AM: mycorrhizal 597

plants; NM: nonmycorrhizal plants. (a, b) Total biomass (dry weight, DW). (c, d) K+ 598

concentration in shoots. (e, f) K+ concentration in roots. Error bars indicate SEs (n=5). The 599

asterisk indicates a significant difference (P < 0.05). 600

Figure 9. Effects of overexpression of SlHAK10 on AM colonization efficiency under a 601

sand-based pot culture condition. Two-week-old seedlings were grown in sand-based pot 602

culture for AM fungal inoculation. The plants were treated with either high-K+ (2 mM K+) or 603

low-K+ (0.2 mM K+) solution. The total root length colonization (a) and arbuscule abundance 604

(b) in the mycorrhizal roots of wild-type and SlHAK10-overexpressing plants were assessed 605

at 5 weeks postinoculation (wpi). (c, d) The transcript levels of two AM-related marker genes, 606

SlPT4 (LePT4) and RiTub from tomato and R. irregularis, respectively. Error bars indicate SEs 607

(n=5). The asterisk indicates a significant difference (P < 0.05). 608

Figure 10. The contents of soluble sugar in the WT and SlHAK10-overexpressing plants. 609

Two-week-old seedlings were grown in sand-based pot culture for AM fungal inoculation. 610



34

The plants were treated with either high-K+ (2 mM K+) or low-K+ (0.2 mM K+) solution. The 611

soluble sugar concentrations in the shoots (a, b) and roots (c, d) of wild-type and 612

SlHAK10-overexpressing plants were determined at 5 weeks postinoculation (wpi). Error 613

bars indicate SEs (n=5). The asterisk indicates a significant difference (P < 0.05). 614

615

616

617

618



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https://www.ncbi.nlm.nih.gov/pubmed?term=Aranda%2DSicilia MN%2C Aboukila A%2C Armbruster U%2C Cagnac O%2C Schumann T%2C Kunz HH%2C Jahns P%2C Rodguez%2DRosales MP%2C Sze H%2C Venema K %282016%29 Envelope K%2B%2FH%2B antiporters AtKEA1 and AtKEA2 function in plastid development%2E Plant Physiol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Cakmak I%2C Hengeler C%2C Marschner H %281994a%29 Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus%2C potassium and magnesium deficiency%2E J Exp Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Cakmak I%2C Hengeler C%2C Marschner H %281994b%29 Changes in phloem export of sucrose in leaves in response to phosphorus%2C potassium and magnesium deficiency in bean plants%2E J Exp Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Casieri L%2C Ait%2C Lahmidi N%2C Doidy J%2C Veneault%2DFourrey C%2C Migeon A%2C Bonneau L%2C Courty PE%2C Garcia K%2C Charbonnier M%2C Delteil A%2C Brun A%2C Zimmermann S%2C Plassard C%2C Wipf D%2E %282013%29 Biotrophic transportome in mutualistic plant%2Dfungal interactions%2E Mycorrhiza&dopt=abstract

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https://scholar.google.com/scholar?as_q=Biotrophic transportome in mutualistic plant-fungal interactions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Casieri&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Cellier F%2C Con�j�ro G%2C Ricaud L%2C Luu DT%2C Lepetit M%2C Gosti F%2C Casse F %282004%29 Characterization of AtCHX17%2C a member of the cation%2FH%2B exchangers%2C CHX family%2C from Arabidopsis thaliana suggests a role in K%2B homeostasis%2E Plant J&dopt=abstract

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https://scholar.google.com/scholar?as_q=Genome-wide investigation and expression analysis suggest diverse roles and genetic redundancy of Pht1 family genes in response to Pi deficiency in tomato&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Chen A%2C Gu M%2C Sun S%2C Zhu L%2C Hong S%2C Xu G %282011%29 Identification of two conserved cis%2Dacting elements%2C MYCS and P1BS%2C involved in the regulation of mycorrhiza %2Dactivated phosphate transporters in eudicot species%2E New Phytol&dopt=abstract


https://scholar.google.com/scholar?as_q=Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza -activated phosphate transporters in eudicot species&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza -activated phosphate transporters in eudicot species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Chen A%2C Hu J%2C Sun S%2C Xu G %282007%29 Conservation and divergence of both phosphate%2D and mycorrhiza%2Dregulated physiological responses and expression patterns of phosphate transporters in solanaceous species%2E New Phytol&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Nagy R%2C Vasconcelos MJ%2C Zhao S%2C McElver J%2C Bruce W%2C Amrhein N%2C Raghothama KG%2C Bucher M%2E 2006%2E Differential regulation of five Pht1 phosphate transporters from maize %28Zea mays L%2E%29%2E Plant Biology&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Nieves%2DCordones M%2C R�denas R%2C Chavanieu A%2C Rivero RM%2C Martinez V%2C Gaillard I%2C Rubio F %282016%29 Uneven HAK%2FKUP%2FKT protein diversity among angiosperms%3A species distribution and perspectives%2E Front Plant Sci&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Oldroyd GE %282013%29 Speak%2C friend%2C and enter%3A signaling systems that promote beneficial symbiotic associations in plants%2E Nat Rev Microbiol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Arbuscular mycorrhizal fungi are an alternative to the application of chemical fertilizer in the production of the medicinal and aromatic plant Coriandrum sativum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Oliveira&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Osakabe Y%2C Arinaga N%2C Umezawa N%2C Katsura S%2C Nagamachi K%2C Tanaka H%2C Ohiraki H%2C Yamada K%2C Seo SU%2C Abo M%2C Yoshimura E%2C Shinozaki K%2C Yamaguchi%2DShinozakia K %282013%29 Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis%2E Plant cell&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Smith SE%2C Smith FA %282011%29 Roles of arbuscular mycorrhiza in plant nutrition and growth%3A new paradigms from cellular to ecosystem scales%2E Annu Rev Plant Biol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Smith SE%2C Smith FA %282012%29 Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth%2E Mycologia&dopt=abstract


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https://scholar.google.com/scholar?as_q=Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smith&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Smith SE%2C Smith FA%2C Jakobsen I %282003%29 Functional diversity in arbuscular mycorrhizal %28AM%29 symbioses%3A the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake%2E New Phytol&dopt=abstract


https://scholar.google.com/scholar?as_q=Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smith&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Sugimura Y %26 Saito K %282017%29 Comparative transcriptome analysis between Solanum lycopersicum L%2E and Lotus japonicus L%2E during arbuscular mycorrhizal development%2E Soil Sci Plant Nutr&dopt=abstract

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https://scholar.google.com/scholar?as_q=Comparative transcriptome analysis between Solanum lycopersicum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sugimura&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Sun HJ%2C Uchii S%2C atanabe S%2C Ezura H %282006%29 A highly efficient transformation protocol for Micro%2DTom%2C a model cultivar for tomato functional genomics%2E Plant Cell Physiol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Sun HW%2C Tao JY%2C Liu SJ%2C Huang SJ%2C Chen S%2C Xie XN%2C Yoneyama K%2C Zhang YL%2C Xu GH %282014%29 Strigolactones are involved in phosphate%2D and nitrate%2Ddeficiency%2Dinduced root development and auxin transport in rice%2E J Exp Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Takahashi R%2C Liu S%2C Takano T %282007%29 Cloning and functional comparison of a high%2Daffinity K%2B transporter gene PhaHKT1 of salt%2Dtolerant and salt%2Dsensitive reed plants%2E J Exp Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Uozumi N%2C Kim EJ%2C Rubio F%2C Yamaguchi T%2C Muto S%2C Tsuboi A%2C Bakker EP%2C Nakamura T%2C Schroeder JI %282000%29 The Arabidopsis HKT1 gene homologue mediates inward Na%2B currents in Xenopus laevis oocytes and Na%2B uptake in Saccharomyces cerevisiae%2E Plant Physiol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Voelker C%2C Schmidt D%2C Mueller%2DRoeber B%2C Czempinski K %282006%29 Members of the Arabidopsis AtTPK%2FKCO family form homomeric vacuolar channels in planta%2E Plant J&dopt=abstract

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https://scholar.google.com/scholar?as_q=Potassium transport and signaling in higher plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wang Y%2C Wu WH %282017%29 Regulation of potassium transport and signaling in plants%2E Curr Opin Plant Biol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Regulation of potassium transport and signaling in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Regulation of potassium transport and signaling in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


White PJ (2013) Improving potassium acquisition and utilization by crop plants. J Plant Nutr Soil Sci 176: 305-316.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Xie XA, Huang W, Liu FC, Tang NW, Liu Y, Lin H, Zhao B (2012) Functional analysis of the novel mycorrhiza-specific phosphatetransporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytol 198: 836-852.


Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S,Mattes N, Heuer S, Paszkowski U (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of thePHOSPHATE TRANSPORTER1 gene family. Plant cell 24: 4236-4251.


Yang T, Zhang S, Hu Y, Wu F, Hu Q, Chen G, Cai J, Wu T, Moran N,Yu L, Xu G (2014) The role of a potassium transporter OsHAK5 inpotassium acquisition and transport from roots to shoots in rice at low potassium supply levels. Plant Physiol 166: 945-959.


Yang Z, Gao Q, Sun C, Li W, Gu S, Xu C (2009) Molecular evolution and functional divergence of HAK potassium transporter genefamily in rice (Oryza sativaL.). J Genet Genomics 36: 161-172.


Zhang HQ, Wei SZ, Hu WT, Xiao LM, Tang M (2017) Arbuscular Mycorrhizal Fungus Rhizophagus irregularis increased potassiumcontent and expression of genes encoding potassium channels in Lycium barbarum. Front in Plant Sci 8: 440.



https://www.ncbi.nlm.nih.gov/pubmed?term=White PJ %282013%29 Improving potassium acquisition and utilization by crop plants%2E J Plant Nutr Soil Sci&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=White&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Improving potassium acquisition and utilization by crop plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Improving potassium acquisition and utilization by crop plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=White&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Xie XA%2C Huang W%2C Liu FC%2C Tang NW%2C Liu Y%2C Lin H%2C Zhao B %282012%29 Functional analysis of the novel mycorrhiza%2Dspecific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis%2E New Phytol&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Xie&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xie&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yang SY%2C Gr�nlund M%2C Jakobsen I%2C Grotemeyer MS%2C Rentsch D%2C Miyao A%2C Hirochika H%2C Kumar CS%2C Sundaresan V%2C Salamin N%2C Catausan S%2C Mattes N%2C Heuer S%2C Paszkowski U %282012%29 Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family%2E Plant cell&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yang T%2C Zhang S%2C Hu Y%2C Wu F%2C Hu Q%2C Chen G%2C Cai J%2C Wu T%2C Moran N%2CYu L%2C Xu G %282014%29 The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels%2E Plant Physiol&dopt=abstract


https://scholar.google.com/scholar?as_q=The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yang Z%2C Gao Q%2C Sun C%2C Li W%2C Gu S%2C Xu C %282009%29 Molecular evolution and functional divergence of HAK potassium transporter gene family in rice %28Oryza sativaL%2E%29%2E J Genet Genomics&dopt=abstract


https://scholar.google.com/scholar?as_q=Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativaL&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Molecular evolution and functional divergence of HAK potassium transporter gene family in rice (Oryza sativaL&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Zhang HQ%2C Wei SZ%2C Hu WT%2C Xiao LM%2C Tang M %282017%29 Arbuscular Mycorrhizal Fungus Rhizophagus irregularis increased potassium content and expression of genes encoding potassium channels in Lycium barbarum%2E Front in Plant Sci&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Arbuscular Mycorrhizal Fungus Rhizophagus irregularis increased potassium content and expression of genes encoding potassium channels in Lycium barbarum&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Arbuscular Mycorrhizal Fungus Rhizophagus irregularis increased potassium content and expression of genes encoding potassium channels in Lycium barbarum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


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