植物对缺磷和铝毒协同进化应答的分子生理机制

doi:10.13560/j.cnki.biotech.bull.1985.2019-1211

摘要/Abstract

摘要： 酸性土壤占世界潜耕性土壤的50%,而缺磷（P）和铝（Al）毒是酸性土壤限制植物生长的两大营养逆境因子。有机酸、激素和铁（Fe）稳态在植物响应2种胁迫的信号交互和协同进化中扮演核心作用。系统综述了有机酸分泌、STOP1/ALMT1和STAR1/ALS3多效性调节、激素信号转导和细胞壁相关激酶在调控植物根发育和根构型以改善酸性土壤P有效性和Al耐性的分子生理机制,并对该领域发展前景进行了展望。

关键词: 酸性土壤, 缺磷, 铝毒, 信号交互, 胁迫应答

Abstract: Acid soils comprise approximately 50% of potential arable lands worldwide. Phosphorus（P）deficiency and aluminum（Al）toxicity are two major nutritional stress factors limiting plant growth on acid soils. Studies have shown that organic acids（OA）,hormones and iron（Fe）homeostasis play a core role in co-evolution and signal crosstalk of plant responses to both stresses. This article systematically reviewed the physiological and molecular mechanisms of OA secretion,pleiotropic regulation of STOP1/ALMT1 and STAR1/ALS3,hormone signal transduction and cell wall-related kinases in regulating plant root development and root architecture to improve P availability and Al resistance on acid soils and also prospected the visions in this field.

Key words: acid soils, phosphorus deficiency, aluminum toxicity, signal crosstalk, stress response

吴佩, 李浩, 早浩龙, 王宇蕴, 杨建立, 汤利, 范伟. 植物对缺磷和铝毒协同进化应答的分子生理机制[J]. 生物技术通报, 2020, 36(7): 170-181.

WU Pei, LI Hao, ZAO Hao-long, WANG Yu-yun, YANG Jian-li, TANG Li, FAN Wei. Physiological and Molecular Mechanisms of Plant Co-evolution Responses to Phosphorous Deficiency and Aluminum Toxicity[J]. Biotechnology Bulletin, 2020, 36(7): 170-181.

参考文献

[1] Von Uexkull HR, Mutert E.Global extent, development and economic impact of acid soils[J]. Plant Soil, 1995, 171(1):1-15.
[2] Ma JF, Chen ZC, Shen RF.Molecular mechanisms of Al tolerance in gramineous plants[J]. Plant Soil, 2014, 381(1/2):1-12.
[3] Kochian LV, Hoekenga OA, Pineros MA.How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency[J]. Annu Rev Plant Biol, 2004, 55:459-493.
[4] Zheng SJ.Crop production on acidic soils:overcoming aluminium toxicity and phosphorus deficiency[J]. Ann Bot, 2010, 106(1):183-184.
[5] Ma JF.Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants[J]. Int Rev Cytol, 2007, 264:225-252.
[6] Cheng L, Bucciarelli B, Shen J, et al.Update on white lupin cluster root acclimation to phosphorus deficiency[J]. Plantm Physiol, 2011, 156(3):1025-1032.
[7] Puga MI, Rojas-Triana M, De Lorenzo L, et al.Novel signals in the regulation of Pi starvation responses in plants:facts and promises[J]. Curr Opin Plant Biol, 2017, 39:40-49.
[8] Kochian LV, Pineros MA, Liu J, et al.Plant adaptation to acid soils:the molecular basis for crop aluminum resistance[J]. Annu Rev Plant Biol, 2015, 66:571-598.
[9] Yang JL, Fan W, Zheng SJ.Mechanisms and regulation of aluminum-induced secretion of organic acid anions from plant roots[J]. J Zhejlang Univ-Sci B, 2019, 20(6):513-527.
[10] Sasaki T, Yamamoto Y, Ezaki B, et al.A wheat gene encoding an aluminum-activated malate transporter[J]. Plant J, 2004, 37(5):645-653.
[11] Ryan PR, Raman H, Gupta S, et al.A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots[J]. Plant Physiol, 2009, 149(1):340-351.
[12] Tovkach A, Ryan PR, Richardson AE, et al.Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices[J]. Plant Physiol, 2013, 161(2):880-892.
[13] Collins NC, Shirley NJ, Saeed M, et al.An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye(Secale cereale L.)[J]. Genetics, 2008, 179(1):669-682.
[14] Yokosho K, Naoki Yamaji N, Ma JF.Isolation and characterisation of two MATE genes in rye[J]. Funct Plant Biol, 2010, 179(1):669-682.
[15] Hoekenga OA, Maron LG, Piñeros MA, et al.AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis[J]. Proc Natl Acad Sci USA, 2006, 103(25):9738-9743.
[16] Liu J, Magalhaes JV, Shaff J, et al.Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance[J]. Plant J, 2009, 57(3):389-399.
[17] Zhang L, Wu X, Wang J, et al.BoALMT1, an Al-induced malate transporter in cabbage, enhances aluminum tolerance in Arabidopsis thaliana[J]. Front Plant Sci, 2017, 8:2156.
[18] Wu X, Li R, Shi J, et al.Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana[J]. Plant Cell Physiol, 2014, 55(8):1426-1436.
[19] Lei GJ, Yokosho K, Yamaji N, et al.Two MATE transporters with different subcellular localization are involved in Al tolerance in buckwheat[J]. Plant Cell Physiol, 2017, 58(12):2179-2189.
[20] Zheng SJ, Ma JF, Matsumoto H.High aluminum resistance in buckwheat:I. Al-induced specific secretion of oxalic acid from root tips[J]. Plant Physiol, 1998, 117(3):745-751.
[21] Ye J, Wang X, Hu T, et al.An InDel in the promoter of Al-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance[J]. Plant Cell, 2017, 29(9):2249-2268.
[22] Yang JL, Zhang L, Zheng SJ.Aluminum-activated oxalate secretion does not associate with internal content among some oxalate accumulators[J]. J Integr Plant Biol, 2008, 50(9):1103-1107.
[23] Ligaba A, Katsuhara M, Ryan PR, et al.The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells[J]. Plant Physiol, 2006, 142(3):1294-1303.
[24] Chen ZC, Yokosho K, Kashino M, et al.Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus[J]. Plant J, 2013, 76(1):10-23.
[25] Furukawa J, Yamaji N, Wang H, et al.An aluminum-activated citrate transporter in barley[J]. Plant Cell Physiol, 2007, 48(8):1081-1091.
[26] Maron LG, Piñeros MA, Guimarães CT, et al.Two functionally distinct members of the MATE(multi-drug and toxic compound extrusion)family of transporters potentially underlie two major aluminum tolerance QTLs in maize[J]. Plant J, 2010, 61(5):728-740.
[27] Yokosho K, Yamaji N, Ma JF.An Al-inducible MATE gene is involved in external detoxification of Al in rice[J]. Plant J, 2011, 68(6):1061-1069.
[28] Yokosho K, Yamaji N, Fujii-Kashino M, et al.Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice[J]. Plant Cell Physiol, 2016, 57(5):967-985.
[29] Qiu W, Wang N, Dai J, et al.AhFRDL1-mediated citrate secretion contributes to adaptation to iron deficiency and aluminum stress in peanuts[J]. J Exp Bot, 2016, 70(10):2873-2886.
[30] Magalhaes JV, Liu J, Guimarães CT, et al.A gene in the multidrug and toxic compound extrusion(MATE)family confers aluminum tolerance in sorghum[J]. Nat Genet, 2007, 39(9):1156-1161.
[31] Yang XY, Yang JL, Zhou Y, et al.A de novo synthesis citrate tran-sporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al-activated citrate efflux in rice bean(Vigna umbellata)root apex[J]. Plant Cell Environ, 2011, 34(12):2138-2148.
[32] Liu MY, Lou HQ, Chen WW, et al.Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress[J]. Plant Cell Environ, 2018, 41(4):809-822.
[33] Ma Q, Yi R, Li L, et al.GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana[J]. BMC Plant Biol, 2018, 18(1):212.
[34] Ma Z, Miyasaka SC.Oxalate exudation by taro in response to Al[J]. Plant Physiol, 1998, 118(3):861-865.
[35] Yang JL, Zheng SJ, He YF, et al.Aluminium resistance requires resistance to acid stress:a case study with spinach that exudes oxalate rapidly when exposed to Al stress[J]. J Exp Bot, 2005, 56(414):1197-1203.
[36] Liang CY, Piñeros MA, Tian J, et al.Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils[J]. Plant Physiol, 2013, 161(3):1347-1361.
[37] Peng W, Wu W, Peng J, et al.Characterization of the soybean GmALMT family genes and the function of GmALMT5 in response to phosphate starvation[J]. J Integr Plant Biol, 2018, 60(3):216-231.
[38] 申建波, 张福锁, 毛达如. 磷胁迫下大豆根分泌有机酸的动态变化[J]. 中国农业大学学报, 1998, 3(增刊):44-48.
[39] Lipton DS, Blanchar RW, Blevins DG.Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings[J]. Plant Physiol, 1987, 85(2):315-317.
[40] Shen H, Yan X, Zhao M, et al.Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates[J]. Environ Exp Bot, 2002, 48(1):1-9.
[41] Johnson JF, Allan DL, Vance CP.Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus[J]. Plant Physiol, 1994, 104(2):657-665.
[42] Ishikawa S, Adu-Gyamfi JJ, Nakamura T, et al.Genotypic variability in phosphorus solubilizing activity of root exudates by pigeonpea grown in low-nutrient environments[J]. Plant and Soil, 2002, 245:71-81.
[43] Hoffland E, Findenegg GR, Nelemans JA.Solubilization of rock phosphate by rape:II. Local root exudation of organic acids as a response to P-starvation[J]. Plant and Soil, 1989, 113:161-165.
[44] Li XF, Zuo HZ, Ling GZ, et al.Secretion of citrate from roots in response to aluminum and low phosphorus stresses in Stylosanthes[J]. Plant Soil, 2009, 325:219-229.
[45] Kirk GJD, Santos EE, Findenegg GR.Phosphate solubilization by organic anion excretion from rice(Oryza sativa L.)growing in aerobic soil[J]. Plant and Soil, 1999, 211:11-18.
[46] Yang LT, Jiang HX, Qi YP, et al.Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in citrus roots[J]. Mol Biol Rep, 2012, 39(5):6353-6366.
[47] Balzergue C, Dartevelle T, Godon C, et al.Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation[J]. Nat Commun, 2017, 8:15300.
[48] Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, et al.Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate[J]. Proc Natl Acad Sci USA, 2017, 114(17):E3563-E3572.
[49] Tan K, Keltjens WG.Interaction between aluminium and phosphorus in sorghum plants[J]. Plant and Soil, 1990, 124(1):15-23.
[50] Pellet DM, Papernik LA, Kochian LV.Multiple aluminum-resistance mechanisms in wheat(roles of root apical phosphate and malate exudation)[J]. Plant Physiol, 1996, 112(2):591-597.
[51] Dong D, Peng X, Yan X.Organic acid exudation induced by phosphorus deficiency and/or aluminum toxicity in two contrasting soybean genotypes[J]. Physiol Plantarum, 2004, 122(2):190-199.
[52] Ligaba A, Shen H, Shibata K, et al.The role of phosphorus in aluminum-induced citrate and malate exudation from rape(Brassica napus)[J]. Physiologia Plantarum, 2004, 120(4):575-584.
[53] Liao H, Wan H, Shaff J, et al.Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. exudation of specific organic acids from different regions of the intact root system[J]. Plant Physiol, 2006, 141(2):674-684.
[54] Zheng SJ, Yang JL, He YF, et al.Immobilization of aluminum with phosphorus in roots is associated with high aluminum resistance in buckwheat[J]. Plant Physiol, 2005, 138(1):297-303.
[55] Xia JX, Yamaji N, Kasai T, et al.Plasma membrane-localized transporter for aluminum in rice[J]. Proc Natl Acad Sci USA, 2010, 107(43):18381-18385.
[56] Huang CF, Yamaji N, Chen Z, et al.A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice[J]. Plant J, 2012, 69(5):857-867.
[57] Wang Y, Li R, Li D, et al.NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis[J]. Proc Natl Acad Sci USA, 2017, 114(19):5047-5052.
[58] Xu L, Zhao H, Wan R, et al.Identification of vacuolar phosphate efflux transporters in land plants[J]. Nature Plants, 2019, 5(1):84-94.
[59] Piñeros MA, Cancado GMA, Kochian LV.Novel properties of the wheat aluminum tolerance organic acid transporter(TaALMT1)revealed by electrophysiological characterization in Xenopus Oocytes:functional and structural implications[J]. Plant Physiol, 2008, 147(4):2131-2146.
[60] Zhang WH, Ryan PR, Sasaki T, et al.Characterization of the TaALMT1 protein as an Al³+-activated anion channel in transformed tobacco(Nicotiana tabacum L.)cells[J]. Plant Physiol, 2008, 49(9):1316-1330.
[61] Furuichi T, Sasaki T, Tsuchiya Y, et al.An extracellular hydrophilic carboxy-terminal domain regulates the activity of TaALMT1, the aluminum-activated malate transport protein of wheat[J]. Plant J, 2010, 64(1):47-55.
[62] Ligaba A, Dreyer I, Margaryan A, et al.Functional, structural and phylogenetic analysis of domains underlying the Al sensitivity of the aluminum-activated malate/anion transporter, TaALMT1[J]. Plant J, 2013, 76(5):766-780.
[63] Ramesh SA, Kamran M, Sullivan W, et al.Aluminum-activated malate transporters can facilitate GABA transport[J]. Plant Cell, 2018, 30(5):1147-1164.
[64] Ramesh SA, Tyerman SD, Xu B, et al.GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters[J]. Nat Commun, 2015, 6:7879.
[65] Furukawa J, Yamaji N, Wang H, et al.An aluminum-activated citrate transporter in barley[J]. Plant Cell Physiol, 2007, 48(8):1081-1091.
[66] Yokosho K, Yamaji N, Fujii-Kashino M, et al.Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice[J]. Plant Cell Physiol, 2016, 57(5):967-985.
[67] Doshi R, McGrath AP, Piñeros M, et al. Functional characterization and discovery of modulators of SbMATE, the agronomically important aluminium tolerance transporter from Sorghum bicolor[J]. Sci Rep, 2017, 7(1):17996.
[68] Delhaize E, Taylor P, Hocking PJ, et al.Transgenic barley(Hordeum vulgare L.)expressing the wheat aluminium resistance gene(TaALMT1)shows enhanced phosphorus nutrition and grain production when grown on an acid soil[J]. Plant Biotechnol J, 2009, 7(5):391-400.
[69] Sawaki Y, Iuchi S, Kobayashi Y, et al.STOP1 Regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities[J]. Plant Physiol, 2009, 150(1):281-294.
[70] Yamaji N, Huang CF, Nagao S, et al.A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice[J]. Plant Cell, 2009, 21(10):3339-3349.
[71] Chen ZC, Yamaji N, Motoyama R, et al.Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice[J]. Plant Physiol, 2012, 159(4):1624-1633.
[72] Müller J, Toev T, Heisters M, et al.Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability[J]. Dev Cell, 2015, 33(2):216-230.
[73] Zheng Z, Wang Z, Wang XY, et al.Blue light triggered-chemical reactions underlie phosphate deficiency-induced inhibition of root elongation of Arabidopsis seedlings grown in petri dishes[J]. Mol Plant, 2019, 12(11):1515-1523.
[74] Sánchez-Calderón L, López-Bucio J, Chacón-López A, et al.Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana[J]. Plant Physiol, 2005, 46(1):174-184.
[75] Larsen PB, Geisler MJB, Jones CA, et al.ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis[J]. Plant J, 2005, 41(3):353-363.
[76] Huang CF, Yamaji N, Ma JF.Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis[J]. Plant Physiol, 2010, 153(4):1669-1677.
[77] Larsen PB, Kochian LV, Howell SH.Al inhibits both shoot development and root growth in als3, an Al-sensitive Arabidopsis mutant[J]. Plant Physiol, 1997, 114(4):1207-1214.
[78] Huang CF, Yamaji N, Mitani N, et al.A bacterial-type ABC transporter is involved in aluminum tolerance in rice[J]. Plant Cell, 2009, 21(2):655-667.
[79] Dong J, Piñeros MA, Li X, et al.An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots[J]. Mol Plant, 2017, 10(2):244-259.
[80] Xu JM, Lou HQ, Jin JF, et al.A half-type ABC transporter FeSTAR1 regulates Al resistance possibly via UDP-glucose-based hemicellulose metabolism and Al binding[J]. Plant Soil, 2018, 423:303-314.
[81] Xu JM, Wang ZQ, Jin JF, et al.FeSTAR2 interacted by FeSTAR1 alters its subcellular location and regulates Al tolerance in buckwheat[J]. Plant Soil, 2019, 436(1):489-501.
[82] Wang XY, Wang Z, Zheng Z, et al.Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency[J]. Plant Physiol, 2019, 179(1):300-316.
[83] Zhang Y, Zhang J, Guo JL, et al.F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis[J]. Proc Natl Acad Sci USA, 2019, 116(1):319-327.
[84] Godon C, Mercier C, Wang XY, et al.Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells[J]. Plant J, 2019, 99(5):937-949
[85] Kollmeier M, Felle HH, Horst WJ.Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?[J]. Plant Physiol, 2000, 122(3):945-956.
[86] Doncheva S, Amenos M, Poschenrieder C, et al.Root cell patterning:a primary target for aluminium toxicity in maize[J]. J Exp Bot, 2005, 56(414):1213-1220.
[87] Sun P, Tian QY, Chen J, et al.Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin[J]. J Exp Bot, 2010, 61(2):347-356.
[88] Sánchez-Calderón L, López-Bucio J, Chacón-López A, et al.Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency[J]. Plant Physiol, 2006, 140(3):879-889.
[89] Svistoonoff S, Creff A, Reymond M, et al.Root tip contact with low-phosphate media reprograms plant root architecture[J]. Nat Genet, 2007, 39(6):792-796.
[90] Wang X, Du G, Wang X, et al.The Function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana[J]. Plant Cell Physiol, 2010, 51(3):380-394.
[91] Ruíz-Herrera LF, López-Bucio J.Aluminum induces low phosphate adaptive responses and modulates primary and lateral root growth by differentially affecting auxin signaling in Arabidopsis seedlings[J]. Plant Soil, 2013, 371(1-2):593-609.
[92] Pérez-Torres C A, López-Bucio J, Cruz-Ramírez A, et al. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor[J]. Plant Cell, 2008, 20(12):3258-3272.
[93] Nagarajan VK, Smith AP.Ethylene’s role in phosphate starvation signaling:more than just a root growth regulator[J]. Plant Cell Physiol, 2012, 53(2):277-286.
[94] Song L, Yu H, Dong J, et al.The Molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation[J]. PLoS Genet, 2016, 12(7):e1006194.
[95] Liu G, Gao S, Tian H, et al.Local transcriptional control of YUCCA regulates auxin promoted root-growth inhibition in response to aluminium stress in Arabidopsis[J]. PLoS Genet, 2016, 12(10):e1006360.
[96] Yang ZB, Geng X, He C, et al.TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis[J]. Plant Cell, 2014, 26(7):2889-2904.
[97] Zhang M, Lu X, Li C, et al.Auxin efflux carrier ZmPGP1 mediates root growth inhibition under aluminum stress[J]. Plant Physiol, 2018, 177(20):819-832.
[98] Lei M, Zhu C, Liu Y, et al.Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis[J]. New Phytol, 2011, 189(4):1084-1095.
[99] Yang ZB, Liu G, Liu J, et al.Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis[J]. EMBO Reports, 2017, 18(7):1213-1230.
[100] Khan GA, Vogiatzaki E, Glauser G, et al.Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory[J]. Plant Physiol, 2016, 171(1):632-644.
[101] Yang ZB, He C, Ma Y, et al.Jasmonic acid enhances Al-induced root-growth inhibition[J]. Plant Physiol, 2017, 173(2):1420-1433.
[102] Anderson CM, Wagner TA, Perret M, et al.WAKs:cell wall-associated kinases linking the cytoplasm to the extracellular matrix[J]. Plant Mol Biol, 2001, 47(1/2):197-206.
[103] Sivaguru M, Ezaki B, He ZH, et al.Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis[J]. Plant Physiol, 2003, 132(4):2256-2266.
[104] Lou HQ, Fan W, Jin JF, et al.A NAC-type transcription factor confers aluminum resistance by regulating cell wall-associated receptor kinase 1 and cell wall pectin[J]. Plant Cell Environ, 2020, 43(2):463-478.
[105] Hufnagel B, De Sousa SM, Assis L, et al.Duplicate and conquer:multiple homologs of PHOSPHORUSSTARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils[J]. Plant Physiol, 2014, 166(2):659-677.
[106] Gamuyao R, Chin JH, Pariasca-tanaka J, et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency[J]. Nature, 2012, 488(7412):535-539.
[107] Verica J, He Z.The cell wall-associated kinase(WAK)and WAK-like kinase gene family[J]. Plant Physiol, 2002, 129(2):455-459.
[108] Kohorn BD, Hoon D, Minkoff B, et al.Rapid oligo-galacturonide induced changes in protein phosphorylation in Arabidopsis[J]. Mol Cell Proteomics, 2016, 15(4):1351-1359.