Xyloglucan and the Advances in Its Roles in Plant Tolerance to Stresses

Expand
  • College of Horticulture, South China Agricultural University, Guangzhou 510642, China
First author contact:

These authors contributed equally to this paper

Received date: 2020-02-10

  Accepted date: 2020-05-08

  Online published: 2020-05-12

Abstract

Xyloglucan (XyG) is a matrix polysaccharide present in the cell wall of all land plants. It is the most abundant hemicellulose in the primary cell walls of dicots (20%-25%, w/w). As a very important plant cell wall component, XyG is not only involved in plant growth and development, but also plays important roles in responses of plants to various abiotic and biotic stresses. The use of genes involved in XyG biosynthesis and degradation possibly improve the tolerance of plants to stresses through influencing the cell wall structure (remodelling) and compositions. In addition, XyG and XyG oligosaccharides likely act as signaling molecules or cooperate with other signaling molecules to induce plant resistance. Here, we review the structure and variety of XyG, the genes involved in XyG biosynthesis and degradation, and advances in potential roles of XyG and XyG-related genes in responses to biotic and abiotic stresses.

Cite this article

Yingyan Xiao, Weina Yuan, Jing Liu, Jian Meng, Qiming Sheng, Yehuan Tan, Chunxiang Xu . Xyloglucan and the Advances in Its Roles in Plant Tolerance to Stresses[J]. Chinese Bulletin of Botany, 2020 , 55(6) : 777 -787 . DOI: 10.11983/CBB20020

References

[1] 陈昆松, 李方, 张上隆 (1999). 猕猴桃果实成熟进程中木葡聚糖内糖基转移酶mRNA水平的变化. 植物学报 41, 1231-1234.
[2] 李雄彪, 张金忠 (1994). 半纤维素的化学结构和生理功能. 植物学通报 11, 27-33.
[3] 刘静 (2018). 低温胁迫对香蕉(Musa spp.)细胞壁半纤维素代谢的影响. 硕士论文. 广州: 华南农业大学. pp. 1-47.
[4] 解敏敏, 晁江涛, 孔英珍 (2015). 参与木葡聚糖合成的糖基转移酶基因研究进展. 植物学报 50, 644-651.
[5] Bacete L, Mélida H, Miedes E, Molina A (2018). Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93, 614-636.
[6] Bai S, Dong CH, Zhu J, Zhang YG, Dai HY (2015). Identification of a xyloglucan-specific endo-(1-4)-beta-D-glucanase inhibitor protein from apple ( Malus × domestica Borkh.) as a potential defense gene against Botryos- phaeria dothidea. Plant Sci 231, 11-19.
[7] Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008). Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20, 1519-1537.
[8] Cho SK, Kim JE, Park JA, Eom TJ, Kim WT (2006). Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580, 3136-3144.
[9] Choi HW, Kim NH, Lee YK, Hwang BK (2013). The pepper extracellular xyloglucan-specific endo-β-1,4-glucanase inhibitor protein gene, CaXEGIP1, is required for plant cell death and defense responses. Plant Physiol 161, 384-396.
[10] Choi JY, Seo YS, Kim SJ, Kim WT, Shin JS (2011). Constitutive expression of CaXTH3, a hot pepper xyloglucan endotransglucosylase/hydrolase, enhanced tolerance to salt and drought stresses without phenotypic defects in tomato plants ( Solanum lycopersicum cv. Dotaerang). Plant Cell Rep 30, 867-877.
[11] Claverie J, Balacey S, Lema?tre-Guillier C, Brulé D, Chiltz A, Granet L, Noirot E, Daire X, Darblade B, Héloir M, Poinssot B (2018). The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front Plant Sci 9, 1725.
[12] Cocuron JC, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel N, Wilkerson CG (2007). A gene from the cellulose synthase-like C family encodes a β-1,4-glucan synthase. Proc Natl Acad Sci USA 104, 8550-8555.
[13] DeBoy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H, Emerson JB, Mohamoud Y, Watkins K, Henrissat B, Gilbert HJ, Nelson KE (2008). Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J Bacteriol 190, 5455-5463.
[14] Del Bem LEV, Vincentz MG (2010). Evolution of xyloglucan-related genes in green plants. BMC Evol Biol 10, 341.
[15] Delvas N, Bauce E, Labbé C, Ollevier T, Bélanger R (2011). Phenolic compounds that confer resistance to spruce budworm. Entomol Exp Appl 141, 35-44.
[16] Divol F, Vilaine F, Thibivilliers S, Kusiak C, Sauge MH, Dinant S (2007). Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environ 30, 187-201.
[17] Dong JL, Jiang YY, Chen RJ, Xu ZJ, Gao XL (2011). Isolation of a novel xyloglucan endotransglucosylase ( OsXET9) gene from rice and analysis of the response of this gene to abiotic stresses. Afr J Biotechnol 10, 17424-17434.
[18] Engelsdorf T, Gigli-Bisceglia N, Veerabagu M, McKenna JF, Vaahtera L, Augstein F, Van der Dose D, Zipfel C, Hamann T (2018). The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci Signal 11, eaao3070.
[19] Faik A, Price NJ, Raikhel NV, Keegstra K (2002). An Arabidopsis gene encoding an α-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci USA 99, 7797-7802.
[20] Franková L, Fry SC (2013). Biochemistry and physiological roles of enzymes that ‘cut and paste’ plant cell-wall polysaccharides. J Exp Bot 64, 3519-3550.
[21] Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau JP, Kato Y, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, Reid JSG, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993). An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89, 1-3.
[22] Gille S, de Souza A, Xiong GY, Benz M, Cheng K, Schultink A, Reca IB, Pauly M (2011). O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. . Plant Cell 23, 4041-4053.
[23] Gille S, Pauly M (2012). O-acetylation of plant cell wall polysaccharides. Front Plant Sci 3, 12.
[24] González-Pérez L, Perrotta L, Acosta A, Orellana E, Spadafora N, Bruno L, Bitonti BM, Albani D, Cabrera JC, Francis D, Rogers HJ (2014). In tobacco BY-2 cells xyloglucan oligosaccharides alter the expression of genes involved in cell wall metabolism, signaling, stress responses, cell division and transcriptional control. Mol Biol Rep 41, 6803-6816.
[25] Günl M, Neumetzler L, Kraemer F, de Souza A, Schultink A, Pena M, York WS, Pauly M (2011). AXY8 encodes an α-fucosidase, underscoring the importance of apoplastic metabolism on the fine structure of Arabidopsis cell wall polysaccharides. Plant Cell 23, 4025-4040.
[26] Han YS, Sa G, Sun J, Shen ZD, Zhao R, Ding MQ, Deng SR, Lu YJ, Zhang YH, Shen X, Chen SL (2014). Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco. Environ Exp Bot 100, 74-83.
[27] Han YS, Wang W, Sun J, Ding MQ, Zhao R, Deng SR, Wang FF, Hu Y, Wang Y, Lu YJ, Du LP, Hu ZM, Diekmann H, Shen X, Polle A, Chen SL (2013). Populus euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants. J Exp Bot 64, 4225-4238.
[28] Hayashi T, Marsden MPF, Delmer DP (1987). Pea xyloglucan and cellulose: VI. Xyloglucan-cellulose interactions in vitro and in vivo. Plant Physiol 83, 384-389.
[29] Hayashi T, Wong YS, Maclachlan G (1984). Pea xyloglucan and cellulose: II. Hydrolysis by pea endo-1,4-β-glucanases. Plant Physiol 75, 605-610.
[30] Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016). The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci 7, 984.
[31] Hu KM, Cao JB, Zhang J, Xia F, Ke YG, Zhang HT, Xie WY, Liu HB, Cui Y, Cao YL, Sun XL, Xiao JH, Li XH, Zhang QL, Wang SP (2017). Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat Plants 3, 17009.
[32] Iurlaro A, De Caroli M, Sabella E, De Pascali M, Rampino P, De Bellis L, Perrotta C, Dalessandro G, Piro G, Fry SC, Lenucci MS (2016). Drought and heat differentially affect XTH expression and XET activity and action in 3-day-old seedlings of durum wheat cultivars with different stress susceptibility. Front Plant Sci 7, 1686.
[33] Jensen JK, Schultink A, Keegstra K, Wilkerson CG, Pauly M (2012). RNA-Seq analysis of developing nasturtium seeds ( Tropaeolum majus): identification and characterization of an additional galactosyltransferase involved in xyloglucan biosynthesis. Mol Plant 5, 984-992.
[34] Jones RW, Ospina-Giraldo M, Deahl K (2006). Gene silencing indicates a role for potato endoglucanase inhibitor protein in germplasm resistance to late blight. Am J Potato Res 83, 41-46.
[35] Karczmarek A, Fudali S, Lichocka M, Sobczak M, Kurek W, Janakowski S, Roosien J, Golinowski W, Bakker J, Goverse A, Helder J (2008). Expression of two functionally distinct plant endo-β-1,4-glucanases is essential for the compatible interaction between potato cyst nematode and its hosts. Mol Plant Microbe Interact 21, 791-798.
[36] Khazaei M, Maali-Amiri R, Talei AR, Ramezanpour S (2015). Differential transcript accumulation of dhydrin and beta-glucosidase genes to cold-induced oxidative stress in chickpea. J Agric Sci Technol 17, 725-734.
[37] Kiefer LL, York WS, Darvill AG, Albersheim P (1989). Xyloglucan isolated from suspension-cultured sycamore cell walls is O-acetylated. Phytochemistry 28, 2105-2107.
[38] Kong YZ, Pe?a MJ, Renna L, Avci U, Pattathil S, Tuomivaara ST, Li XM, Reiter WD, Brandizzi F, Hahn MG, Darvill AG, York WS, O'Neill MA (2015). Galactose-depleted xyloglucan is dysfunctional and leads to dwarfism in Arabidopsis. Plant Physiol 167, 1296-1306.
[39] Kuluev B, Mikhaylova E, Berezhneva Z, Nikonorov Y, Postrigan B, Kudoyarova G, Chemeris A (2017). Expression profiles and hormonal regulation of tobacco NtEXGT gene and its involvement in abiotic stress response. Plant Physiol Biochem 111, 203-215.
[40] Kumar M, Chauhan AS, Kumar M, Yusuf MA, Sanyal I, Chauhan PS (2019). Transcriptome sequencing of chickpea ( Cicer arietinum L.) genotypes for identification of drought-responsive genes under drought stress condition. Plant Mol Biol Rep 37, 186-203.
[41] Li Q, Hu AH, Dou WF, Qi JJ, Long Q, Zou XP, Lei TG, Yao LX, He YR, Chen SC (2019). Systematic analysis and functional validation of citrus XTH genes reveal the role of Csxth04 in citrus bacterial canker resistance and tolerance. Front Plant Sci 10, 1109.
[42] Liang Y, Basu D, Pattathil S, Xu WL, Venetos A, Martin SL, Faik A, Hahn MG, Showalter AM (2013). Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis. J Exp Bot 64, 5537-5551.
[43] Liu LF, Hsia MM, Dama M, Vogel J, Pauly M (2016). A xyloglucan backbone 6- O-acetyltransferase from Brachypodium distachyon modulates xyloglucan xylosylation. Mol Plant 9, 615-617.
[44] Liu LF, Paulitz J, Pauly M (2015). The presence of fucogalactoxyloglucan and its synthesis in rice indicates conserved functional importance in plants. Plant Physiol 168, 549-560.
[45] Ma L, Jiang S, Lin GM, Cai JH, Ye XX, Chen HB, Li MH, Li HP, Taká? T, ?amaj J, Xu CX (2013). Wound-induced pectin methylesterases enhance banana ( Musa spp. AAA) susceptibility to Fusarium oxysporum f. sp cubense. J Exp Bot 64, 2219-2229.
[46] Ma ZC, Zhu L, Song TQ, Wang Y, Zhang Q, Xia YQ, Qiu M, Lin YC, Li HY, Kong L, Fang YF, Ye WW, Wang Y, Dong SM, Zheng XB, Tyler BM, Wang YC (2017). A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355, 710-714.
[47] Mageroy MH, Parent G, Germanos G, Giguère I, Delvas N, Maaroufi H, Bauce é, Bohlmann J, Mackay JJ (2015). Expression of the β-glucosidase gene Pgβglu-1 underpins natural resistance of white spruce against spruce budworm. Plant J 81, 68-80.
[48] Manabe Y, Nafisi M, Verhertbruggen Y, Orfila C, Gille S, Rautengarten C, Cherk C, Marcus SE, Somerville S, Pauly M, Knox JP, Sakuragi Y, Scheller HV (2011). Loss-of-function mutation of REDUCED WALL ACETYLATION 2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol 155, 1068-1078.
[49] Mansoori N, Schultink A, Schubert J, Pauly M (2015). Expression of heterologous xyloglucan xylosyltransferases in Arabidopsis to investigate their role in determi- ning xyloglucan xylosylation substitution patterns. Planta 241, 1145-1158.
[50] Nafisi M, Stranne M, Fimognari L, Atwell S, Martens HJ, Pedas PR, Hansen SF, Nawrath C, Scheller HV, Kliebenstein DJ, Sakuragi Y (2015). Acetylation of cell wall is required for structural integrity of the leaf surface and exerts a global impact on plant stress responses. Front Plant Sci 6, 550.
[51] Niu YQ, Hu B, Li XQ, Chen HB, Taká? T, ?amaj J, Xu CX (2018). Comparative digital gene expression analysis of tissue-cultured plantlets of highly resistant and susceptible banana cultivars in response to Fusarium oxysporum. Int J Mol Sci 19, 350.
[52] Otulak-Kozie? K, Kozie? E, Bujarski JJ (2018). Spatiotemporal changes in xylan-1/xyloglucan and xyloglucan xyloglucosyl transferase (XTH-Xet5) as a step-in of ultrastructural cell wall remodelling in potato-potato virus Y (PVYNTN) hypersensitive and susceptible reaction. Int J Mol Sci 19, 2287.
[53] Pauly M, Keegstra K (2016). Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol 67, 235-259.
[54] Pauly M, Ramírez V (2018). New insights into wall polysaccharide O-acetylation. Front Plant Sci 9, 1210.
[55] Pawar PMA, Ratke C, Balasubramanian VK, Chong SL, Gandla ML, Adriasola M, Sparrman T, Hedenstr?m M, Szwaj K, Derba-Maceluch M, Gaertner C, Mouille G, Ezcurra I, Tenkanen M, J?nsson LJ, Mellerowicz EJ (2017). Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification. New Phytol 214, 1491-1505.
[56] Pe?a MJ, Kong YZ, York WS, O’Neill MA (2012). A galacturonic acid-containing xyloglucan is involved in Arabi-dopsis root hair tip growth. Plant Cell 24, 4511-4524.
[57] Pogorelko G, Lionetti V, Fursova O, Sundaram RM, Qi MS, Whitham SA, Bogdanove AJ, Bellincampi D, Zabotina OA (2013). Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidu- lans acetylesterases have decreased degree of polysacc- haride acetylation and increased resistance to pathogens. Plant Physiol 162, 9-23.
[58] Purugganan MM, Braam J, Fry SC (1997). The Arabidopsis TCH4 xyloglucan endotransglycosylase: substrate specificity, pH optimum, and cold tolerance. Plant Physiol 115, 181-190.
[59] Rao XL, Dixon RA (2017). Brassinosteroid mediated cell wall remodeling in grasses under abiotic stress. Front Plant Sci 8, 806.
[60] Rose JKC, Braam J, Fry SC, Nishitani K (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43, 1421-1435.
[61] Rui Y, Anderson CT (2016). Functional analysis of cellulose and xyloglucan in the walls of stomatal guard cells of Arabidopsis. Plant Physiol 170, 1398-1419.
[62] Sampedro J, Gianzo C, Iglesias N, Guitián E, Revilla G, Zarra I (2012). AtBGAL10 is the main xyloglucan β-galac-tosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158, 1146-1157.
[63] Sampedro J, Valdivia ER, Fraga P, Iglesias N, Revilla G, Zarra I (2017). Soluble and membrane-bound β-glucosidases are involved in trimming the xyloglucan backbone. Plant Physiol 173, 1017-1030.
[64] Scheller HV, Ulvskov P (2010). Hemicelluloses. Annu Rev Plant Biol 61, 263-289.
[65] Schultink A, Cheng K, Park YB, Cosgrove DJ, Pauly M (2013). The identification of two arabinosyltransferases from tomato reveals functional equivalency of xyloglucan side chain substituents. Plant Physiol 163, 86-94.
[66] Schultink A, Naylor D, Dama M, Pauly M (2015). The role of the plant-specific ALTERED XYLOGLU-CAN 9 protein in Arabidopsis cell wall polysaccharide O-acetylation. Plant Physiol 167, 1271-1283.
[67] Sharmin S, Azam MS, Islam MS, Sajib AA, Mahmood N, Hasan AMM, Ahmed R, Sultana K, Khan H (2012). Xyloglucan endotransglycosylase/hydrolase genes from a susceptible and resistant jute species show opposite expression pattern following Macrophomina phaseolina infection. Commun Integr Biol 5, 598-606.
[68] Shigeyama T, Watanabe A, Tokuchi K, Toh S, Sakurai N, Shibuya N, Kawakami N (2016). α-xylosidase plays essential roles in xyloglucan remodelling, maintenance of cell wall integrity, and seed germination in Arabidopsis thaliana. J Exp Bot 67, 5615-5629.
[69] Shinohara N, Sunagawa N, Tamura S, Yokoyama R, Ueda M, Igarashi K, Nishitani K (2017). The plant cell-wall enzyme AtXTH3 catalyses covalent cross-linking between cellulose and cello-oligosaccharide. Sci Rep 7, 46099.
[70] Song L, Valliyodan B, Prince S, Wan JR, Nguyen HT (2018). Characterization of the XTH gene family: new insight to the roles in soybean flooding tolerance. Int J Mol Sci 19, 2705.
[71] Subíkova V, Slovakova L, Farkas V (1994). Inhibition of tobacco necrosis virus infection by xyloglucan fragments. Z Pflanzenk Pflanzen 101, 128-131.
[72] Takahashi D, Gorka M, Erban A, Graf A, Kopka J, Zuther E, Hincha DK (2019). Both cold and sub-zero acclimation induce cell wall modification and changes in the extracellular proteome in Arabidopsis thaliana. Sci Rep 9, 2289.
[73] Thorlby G, Fourrier N, Warren G (2004). The SENSITIVE TO FREEZING 2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a β-glucosidase. Plant Cell 16, 2192-2203.
[74] Vaahtera L, Schulz J, Hamann T (2019). Cell wall integrity maintenance during plant development and interaction with the environment. Nat Plants 5, 924-932.
[75] Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter WD (2002). The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proc Natl Acad Sci USA 99, 3340-3345.
[76] Wang C, Li S, Ng S, Zhang BC, Zhou YH, Whelan J, Wu P, Shou HX (2014). Mutation in xyloglucan 6-xylosytransferase results in abnormal root hair development in Oryza sativa. J Exp Bot 65, 4149-4157.
[77] Wang M, Xu ZC, Ding AM, Kong YZ (2018). Genome-wide identification and expression profiling analysis of the xyloglucan endotransglucosylase/hydrolase gene family in tobacco ( Nicotiana tabacum L.). Genes 9, 273.
[78] Wu YL, Fan W, Li XQ, Chen HB, Taká? T, ?amajová O, Fabrice MR, Xie L, Ma J, ?amaj J, Xu CX (2017). Expression and distribution of extensins and AGPs in susceptible and resistant banana cultivars in response to wounding and Fusarium oxysporum. Sci Rep 7, 42400.
[79] Xie DS, Ma L, ?amaj J, Xu CX (2011). Immunohistochemical analysis of cell wall hydroxyproline-rich glycoproteins in the roots of resistant and susceptible wax gourd cultivars in response to Fusarium oxysporum f. sp. benincasae infection and fusaric acid treatment. Plant Cell Rep 30, 1555-1569.
[80] Xu H, Ding AM, Chen SH, Marowa P, Wang D, Chen M, Hu RB, Kong YZ, O’Neill M, Chai GH, Zhou GK (2018). Genome-wide analysis of Sorghum GT47 family reveals functional divergences of MUR3-like genes. Front Plant Sci 9, 1773.
[81] Yan JW, Huang Y, He H, Han T, Di PC, Sechet J, Fang L, Liang Y, Scheller HV, Mortimer JC, Ni L, Jiang MY, Hou XL, Zhang AY (2019). Xyloglucan endotransglucosylase-hydrolase 30 negatively affects salt tolerance in Arabidopsis. J Exp Bot 70, 5495-5506.
[82] Yan YL, Taká? T, Li XQ, Chen HB, Wang YY, Xu EF, Xie L, Su ZH, ?amaj J, Xu CX (2015). Variable content and distribution of arabinogalactan proteins in banana ( Musa spp.) under low temperature stress. Front Plant Sci 6, 353.
[83] Zhu WJ, Ronen M, Gur Y, Minz-Dub A, Masrati G, Ben-Tal N, Savidor A, Sharon I, Eizner E, Valerius O, Braus GH, Bowler K, Bar-Peled M, Sharon A (2017). BcXYG1, a secreted xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses. Plant Physiol 175, 438-456.
[84] Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhuo YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012). XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24, 4731-4747.
Outlines

/