Abstract
Purpose
Controlling root-to-shoot Cl− transport to reduce Cl− accumulation in shoots is one of crucial mechanisms for salt tolerance of glycophytes, but the proteins directly involved in this process under salt stress are poorly reported. Here, we evaluated the role of Aluminum-activated Malate Transporter 12 (AtALMT12), which is expressed in both guard cells and root steles, in root-to-shoot Cl− transport.
Methods
The expression of AtALMT12 under salt stress was analyzed. The salt tolerance, ion accumulation, and expression of key ion transport genes in roots were compared among wild-type, atalmt12 mutants, and ALMT12 complementation lines driven by a guard cell-specific or a root stele-specific promoter.
Results
The expression of AtALMT12 in roots was significantly induced by Cl−-salt treatment. The mutation of AtALMT12 significantly increased Cl− accumulation and decreased NO3− accumulation in shoots, and reduced plant’s tolerance to Cl−-salt stress. Complementation by AtALMT12 driven by a root stele-specific promoter restored the shoot Cl− and NO3− concentration of atalmt12 mutant to the wild-type level, while AtALMT12 expression driven by a guard cell-specific promoter had no such effect. Meanwhile, loss-of-function of AtALMT12 resulted in an increased expression of AtNPF7.2/NRT1.8 in roots under Cl−-salt stress. In addition, AtALMT12 mutation decreased shoot K+ concentration and the expression of AtSKOR in roots under high KCl treatment.
Conclusions
AtALMT12 participates in restricting root-to-shoot Cl− transport, and modulates NO3− accumulation in shoots under Cl−-salt stress, therefore plays an important role in salt tolerance. Meanwhile, AtALMT12 affects K+ accumulation in shoots under higher KCl condition.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Alnayef M, Solis C, Shabala L, Ogura T, Chen Z, Bose J, Maathuis FJM, Venkataraman G, Tanoi K, Yu M, Zhou M, Horie T, Shabala S (2020) Changes in expression level of OsHKT1;5 alters activity of membrane transporters involved in K+ and Ca2+ acquisition and homeostasis in salinized rice roots. Int J Mol Sci 21:4882. https://doi.org/10.3390/ijms21144882
Ashraf M, Ali Q (2008) Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.). Environ Exp Bot 63:266–273. https://doi.org/10.1016/j.envexpbot.2007.11.008
Baetz U, Eisenach C, Tohge T, Martinoia E, De Angeli A (2016) Vacuolar chloride fluxes impact ion content and distribution during early salinity stress. Plant Physiol 172:1167–1181. https://doi.org/10.1104/pp.16.00183
Bao AK, Du BQ, Touil L, Kang P, Wang QL, Wang SM (2016) Co-expression of tonoplast cation/H+ antiporter and H+-pyrophosphatase from xerophyte Zygophyllum xanthoxylum improves alfalfa plant growth under salinity, drought, and field conditions. Plant Biotechnol J 14:964–975. https://doi.org/10.1111/pbi.12451
Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F, Thomine S, Wege S (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62:25–51. https://doi.org/10.1146/annurev-arplant-042110-103741
Brumós J, Talón M, Bouhlal R, Colmenero-Flores JM (2010) Cl- homeostasis in includer and excluder citrus rootstocks: transport mechanisms and identification of candidate genes. Plant Cell Environ 33:2012–2027. https://doi.org/10.1111/j.1365-3040.2010.02202.x
Cataldo DA, Haroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant-tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80. https://doi.org/10.1080/00103627509366547
Chen ZC, Yamaji N, Fujii-Kashino M, Ma JF (2016) A cation-chloride cotransporter gene is required for cell elongation and osmoregulation in rice. Plant Physiol 171:494–507. https://doi.org/10.1104/pp.16.00017
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Colmenero-Flores JM, Franco-Navarro JD, Cubero-Font P, Peinado-Torrubia P, Rosales MA (2019) Chloride as a beneficial macronutrient in higher plants: new roles and regulation. Int J Mol Sci 20:4686. https://doi.org/10.3390/ijms20194686
Colmenero-Flores JM, Martinez G, Gamba G, Vazquez N, Iglesias DJ, Brumos J, Talon M (2007) Identification and functional characterization of cation-chloride cotransporters in plants. Plant J 50:278–292. https://doi.org/10.1111/j.1365-313X.2007.03048.x
Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200. https://doi.org/10.1016/j.cub.2005.05.048
Conn SJ, Hocking B, Dayod M, Xu B, Athman A, Henderson S, Aukett L, Conn V, Shearer MK, Fuentes S, Tyerman SD, Gilliham M (2013) Protocol: optimising hydroponic growth systems for nutritional and physiological analysis of Arabidopsis thaliana and other plants. Plant Methods 9:4. https://doi.org/10.1186/1746-4811-9-4
Cubero-Font P, Maierhofer T, Jaslan J, Rosales MA, Espartero J, Díaz-Rueda P, Müller HM, Hürter AL, Khaled AS, Marten I, Hedrich R, Colmenero-Flores JM, Geiger D (2016) Silent S-type anion channel subunit SLAH1 gates SLAH3 open for chloride root-to-shoot translocation. Curr Biol 26:2213–2220. https://doi.org/10.1016/j.cub.2016.06.045
Cui YN, Li XT, Yuan JZ, Wang FZ, Guo H, Xia ZR, Wang SM, Ma Q (2020) Chloride is beneficial for growth of the xerophyte Pugionium cornutum by enhancing osmotic adjustment capacity under salt and drought stresses. J Exp Bot 71:4215–4231. https://doi.org/10.1093/jxb/eraa158
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Drechsler N, Zheng Y, Bohner A, Nobmann B, von Wirén N, Kunze R, Rausch C (2015) Nitrate-dependent control of shoot K homeostasis by the nitrate transporter1/peptide transporter family member NPF7.3/NRT1.5 and the stelar K+ outward rectifier SKOR in Arabidopsis. Plant Physiol 169:2832–2847. https://doi.org/10.1104/pp.15.01152
Fort KP, Lowe KM, Thomas WTB, Walker MA (2013) Cultural conditions and propagule type influence relative chloride exclusion in grapevine rootstocks. Am J Enol Viticult 64:241–250. https://doi.org/10.5344/ajev.2013.12073
Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud J, Sentenac H (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655. https://doi.org/10.1016/S0092-8674(00)81606-2
Geilfus CM (2018) Chloride: from nutrient to toxicant. Plant Cell Physiol 59:877–886. https://doi.org/10.1093/pcp/pcy071
Hamburger D, Rezzonico E, Petétot AJM, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902. https://doi.org/10.1105/tpc.000745
Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR, Tyerman SD, Walker RR, Gilliham M (2015) Grapevine and Arabidopsis cation-chloride cotransporters localize to the golgi and trans-golgi network and indirectly influence long-distance ion transport and plant salt tolerance. Plant Physiol 169:2215–2229. https://doi.org/10.1104/pp.15.00499
İbrahimova U, Kumari P, Yadav S, Rastogi A, Antala M, Suleymanova Z, Zivcak M, Tahjib-Ul-Arif M, Hussain S, Abdelhamid M, Hajihashemi S, Yang XH, Brestic M (2021) Progress in understanding salt stress response in plants using biotechnological tools. J Biotechnol 329:180–191. https://doi.org/10.1016/j.jbiotec.2021.02.007
Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434. https://doi.org/10.1146/annurev-arplant-042916-040936
Keisham M, Mukherjee S, Bhatla SC (2018) Mechanisms of sodium transport in plants - progresses and challenges. Int J Mol Sci 19:647. https://doi.org/10.3390/ijms19030647
Li B, Byrt C, Qiu J, Baumann U, Hrmova M, Evrard A, Johnson AAT, Birnbaum KD, Mayo GM, Jha D, Henderson SW, Tester M, Gilliham M, Roy SJ (2016) Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiol 170:1014–1029. https://doi.org/10.1104/pp.15.01163
Li B, Tester M, Gilliham M (2017) Chloride on the move. Trends Plant Sci 22:236–248. https://doi.org/10.1016/j.tplants.2016.12.004
Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassman W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646. https://doi.org/10.1105/tpc.110.075242
Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528. https://doi.org/10.1105/tpc.108.060244
Luo QY, Yu BJ, Liu YL (2005) Differential sensitivity to chloride and sodium ions in seedlings of Glycine max and G. soja under NaCl stress. J Plant Physiol 162:1003–1012. https://doi.org/10.1016/j.jplph.2004.11.008
Ma Q, Hu J, Zhou XR, Yuan HJ, Kumar T, Luan S, Wang SM (2017) ZxAKT1 is essential for K+ uptake and K+/Na+ homeostasis in the succulent xerophyte Zygophyllum xanthoxylum. Plant J 90:48–60. https://doi.org/10.1111/tpj.13465
Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KA, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63:1054–1062. https://doi.org/10.1111/j.1365-313X.2010.04302.x
Møller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178. https://doi.org/10.1105/tpc.108.064568
Munns R, James RA, Gilliham M, Flowers TJ, Colmer TD (2016) Tissue tolerance: an essential but elusive trait for salt-tolerant crops. Funct Plant Biol 43:1103–1113. https://doi.org/10.1071/FP16187
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Munns R, Gilliham M (2015) Salinity tolerance of crops-what is the cost? New Phytol 208:668–673. https://doi.org/10.1111/nph.13519
Pineros MA, Cancado GMA, Kochian LV (2008) Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: functional and structural implications. Plant Physiol 147:2131–2146. https://doi.org/10.1104/pp.108.119636
Qiu J, Henderson SW, Tester M, Roy SJ, Gilliham M (2016) SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl- accumulation and salt tolerance in Arabidopsis thaliana. J Exp Bot 67:4495–4505. https://doi.org/10.1093/jxb/erw237
Raven JA (2017) Chloride: essential micronutrient and multifunctional beneficial ion. J Exp Bot 68:359–367. https://doi.org/10.1093/jxb/erw421
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004
Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K, Matsuoka K, Murata Y, Yamamoto Y (2010) Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol 51:354–365. https://doi.org/10.1093/pcp/pcq016
Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653. https://doi.org/10.1111/j.1365-313X.2003.01991.x
Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938. https://doi.org/10.1111/j.1365-313X.2005.02595.x
Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis. Plant Soil 289:369–383. https://doi.org/10.1007/s11104-006-9146-8
Teakle NL, Tyerman SD (2010) Mechanisms of Cl- transport contributing to salt tolerance. Plant Cell Environ 33:566–589. https://doi.org/10.1111/j.1365-3040.2009.02060.x
Tregeagle JM, Tisdall JM, Tester M, Walker RR (2010) Cl- uptake, transport and accumulation in grapevine rootstocks of differing capacity for Cl- exclusion. Funct Plant Biol 37:665–673. https://doi.org/10.1071/fp09300
Wang Q, Guan C, Wang P, Lv ML, Ma Q, Wu GQ, Zhang JL, Bao AK, Wang SM (2015) AtHKT1;1 and AtHAK5 mediate low-affinity Na+ uptake in Arabidopsis thaliana under mild salt stress. Plant Growth Regul 75:615–623. https://doi.org/10.1007/s10725-014-9964-2
Wang SM, Zhang JL, Flowers TJ (2007) Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiol 145:559–571. https://doi.org/10.1104/pp.107.104315
Wang WY, Liu YQ, Duan HR, Yin XX, Cui YN, Chai WW, Song X, Flowers TJ, Wang SM (2020) SsHKT1;1 is coordinated with SsSOS1 and SsNHX1 to regulate Na+ homeostasis in Suaeda salsa under saline conditions. Plant Soil 449:117–131. https://doi.org/10.1007/s11104-020-04463-x
Wege S, Gilliham M, Henderson SW (2017) Chloride: not simply a ‘cheap osmoticum’, but a beneficial plant macronutrient. J Ex Bot 68:3057–3069. https://doi.org/10.1093/jxb/erx050
Xiao QY, YiChen Y, Liu CW, Robson F, Roy S, Cheng XF, Wen JQ, Mysore K, Anthony J, Miller AJ, Murray JD (2021) MtNPF6.5 mediates chloride uptake and nitrate preference in Medicago roots. EMBO J 40:106847. https://doi.org/10.15252/embj.2020106847
Yuan HJ, Ma Q, Wu GQ, Wang P, Hu J, Wang SM (2015) ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Ann Bot 115:495–507. https://doi.org/10.1093/aob/mcu177
Yin HJ, Li MZ, Lv MH, Hepworth SR, Li DD, Ma CC, Li J, Wang SM (2020) SAUR15 promotes lateral and adventitious root development via activating H+-ATPases and auxin biosynthesis. Plant Physiol 184:837–851. https://doi.org/10.1104/pp.19.01250
Zhao CZ, Heng Zhang H, Song CP, Zhu JK, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. Innovation 1:100017. https://doi.org/10.1016/j.xinn.2020.100017
Zheng Y, Drechsler N, Rausch C, Kunze R (2016) The Arabidopsis nitrate transporter NPF7.3/NRT1.5 is involved in lateral root development under potassium deprivation. Plant Signal Behav 11:5. https://doi.org/10.1080/15592324.2016.1176819
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This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 32171677 and 31730093).
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RWL, JZY and QM conceptualized and designed the study. RWL, JZY, XYL, MMC generated the data. RWL, JZY, YNC and ZHH analyzed the data. RWL, JZY and QM wrote the paper with the help of XYL, YNC, ZHH and MMC.
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Liu, RW., Yuan, JZ., Li, XY. et al. Aluminum-activated Malate Transporter 12 is involved in restricting root-to-shoot Cl− transport in Arabidopsis under Cl−-salt stress. Plant Soil 478, 461–478 (2022). https://doi.org/10.1007/s11104-022-05484-4
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DOI: https://doi.org/10.1007/s11104-022-05484-4