Global identification of genes associated with xylan biosynthesis in cotton fiber

Journal of Cotton Research - Tập 3 - Trang 1-15 - 2020
Feng CHEN1, Yanjun GUO1, Li CHEN1, Xinli GAN1, Min LIU1, Juan LI1, Wenliang XU1,2
1Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan, China
2Zhengzhou Research base, State Key Laboratory of Cotton Biology, Zhengzhou University, Zhengzhou, China

Tóm tắt

Mature cotton fiber secondary cell wall comprises largely of cellulose (> 90%) and small amounts of xylan and lignin. Little is known about the cotton fiber xylan biosynthesis by far. To comprehensively survey xylan biosynthetic genes in cotton fiber, we identified five IRX9, five IRX10, one IRX14, six IRX15, two FRA8, one PARVUS, eight GUX, four GXM, two RWA, two AXY9, 13 TBL genes by using phylogenetic analysis coupled with expression profile analysis and co-expression analyses. In addition, we also identified two GT61 members, two GT47 members, and two DUF579 family members whose homologs in Arabidopsis were not functionally characterized. These 55 genes were regarded as the most probable genes to be involved in fiber xylan biosynthesis. Further complementation analysis indicated that one IRX10 like and two FRA8 related genes were able to partially recover the irregular xylem phenotype conferred by the xylan deficiency in their respective Arabidopsis mutant. We conclude that these genes are functional orthologs of respective genes that are implicated in GX biosynthesis. The list of 55 cotton genes presented here provides not only a solid basis to uncover the biosynthesis of xylan in cotton fiber, but also a genetic resource potentially useful for future studies aiming at fiber improvement via biotechnological approaches.

Tài liệu tham khảo

Anders N, Wilkinson MD, Lovegrove A, et al. Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci U S A. 2012;109(3):989–93. https://doi.org/10.1073/pnas.1115858109. Aspeborg H, Schrader J, Coutinho PM, et al. Carbohydrate-active enzymes involved in the secondary cell wall biogenesis in hybrid Aspen. Plant Physiol. 2005;137:983–97. https://doi.org/10.1104/pp.104.055087. Avci U, Pattathil S, Singh B, et al. Cotton fiber cell walls of Gossypium hirsutum and Gossypium barbadense have differences related to loosely-bound xyloglucan. PLoS One. 2013;8(2):e56315. https://doi.org/10.1371/journal.pone.0056315. Brown DM, Goubet F, Wong VW, et al. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 2007;52:1154–68. https://doi.org/10.1111/j.1365-313X.2007.03307.x. Brown DM, Wightman R, Zhang Z, et al. Arabidopsis genes IRREGULAR XYLEM(IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall. Plant J. 2011;66(3):401–13. https://doi.org/10.1111/j.1365-313X.2011.04501.x. Brown DM, Zhang Z, Stephens E, et al. Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J. 2009;57:732–46. https://doi.org/10.1111/j.1365-313X.2008.03729.x. Egelund J, Skjot M, Geshi N, et al. A complementary bioinformatics approach to identify potential plant cell wall glycosyltransferase-encoding genes. Plant Physiol. 2004;136:2609–20. https://doi.org/10.1104/pp.104.042978. Fan L, Shi WJ, Hu WR, et al. Molecular and biochemical evidence for phenylpropanoid synthesis and presence of wall-linked phenolics in cotton fibers. J Integr Plant Biol. 2009;51(7):626–37. https://doi.org/10.1111/j.1744-7909.2009.00840.x. Gao Y, He C, Zhang D, et al. Two trichome birefringence-like proteins mediate xylan acetylation, which is essential for leaf blight resistance in rice. Plant Physiol. 2017;173:470–81. https://doi.org/10.1104/pp.16.01618. Haigler CH, Betancur L, Stiff MR, et al. Cotton fiber: a powerful single-cell model for cell wall and cellulose research. Front Plant Sci. 2012;3:104. https://doi.org/10.3389/fpls.2012.00104. Han LB, Li YB, Wang HY, et al. The dual functions of WLIM1a in cell elongation and secondary wall formation in developing cotton fibers. Plant Cell. 2013;25:4421–38. https://doi.org/10.1105/tpc.113.116970. Hörnblad E, Ulfstedt M, Ronne H, et al. Partial functional conservation of IRX10 homologs in physcomitrella patens and Arabidopsis thaliana indicates an evolutionary step contributing to vascular formation in land plants. BMC Plant Biol. 2013;13(1):3. https://doi.org/10.1186/1471-2229-13-3. Huang JF, Chen F, Wu SY, et al. Cotton GhMYB7 is predominantly expressed in developing fibers and regulates secondary cell wall biosynthesis in transgenic Arabidopsis. Sci China Life Sci. 2016;59(2):194–205. https://doi.org/10.1007/s11427-015-4991-4. Jensen JK, Johnson NR, Wilkerson CG. Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases. Plant J. 2014;80(2):207–15. https://doi.org/10.1111/tpj.12641. Jensen JK, Kim H, Cocuron JC, et al. The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J. 2011;66:387–400. https://doi.org/10.1111/j.1365-313X.2010.04475.x. Kim H, Ralph J. A gel-state 2D-NMR method for plant cell wall profiling and analysis: a model study with the amorphous cellulose and xylan from ball-milled cotton linters. RSC Adv. 2014;4(15):7549–60. https://doi.org/10.1039/c3ra46338a. Lee C, Teng Q, Huang W, et al. The poplar GT8E and GT8F glycosyltransferases are functional orthologs of Arabidopsis PARVUS involved in glucuronoxylan biosynthesis. Plant Cell Physiol. 2009b;50(11):1982–7. https://doi.org/10.1093/pcp/pcp131. Lee C, Teng Q, Huang WL, et al. The F8H glycosyltransferase is a functional paralog of FRA8 involved in glucuronoxylan biosynthesis in Arabidopsis. Plant Cell Physiol. 2009a;50:812–27. https://doi.org/10.1093/pcp/pcp025. Lee C, Teng Q, Zhong R, et al. The four Arabidopsis REDUCED WALL ACETYLATION genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol. 2011;52(8):1289–301. https://doi.org/10.1093/pcp/pcr075. Lee C, Teng Q, Zhong R, et al. Three Arabidopsis DUF579 domain-containing GXM proteins are methyltransferases catalyzing 4-O-methylation of glucuronic acid on xylan. Plant Cell Physiol. 2012;53(11):1934–49. https://doi.org/10.1093/pcp/pcs138. Lee C, Zhong R, Richardson EA, et al. The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol. 2007;48:1659–72. https://doi.org/10.1093/pcp/pcm155. Lee J, Burns TH, Light GG, et al. Xyloglucan endotransglycosylase/hydrolasegenes in cotton and their role in fiber elongation. Planta. 2010;232:1191–205. https://doi.org/10.1007/s00425-010-1246-2. Li A, Xia T, Xu W, et al. An integrative analysis of four CESA isoforms specific for fiber cellulose production between Gossypium hirsutum and Gossypium barbadense. Planta. 2013;237(6):1585–97. https://doi.org/10.1007/s00425-013-1868-2. Li F, Fan G, Lu C, et al. Genome sequence of cultivated upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol. 2015;33:524–30. https://doi.org/10.1038/nbt.3208. Li L, Huang J, Qin L, et al. Two cotton fiber-associated glycosyltransferases, GhGT43A1 and GhGT43C1, function in hemicellulose glucuronoxylan biosynthesis during plant development. Physiol Plantarum. 2014;152:367–79. https://doi.org/10.1111/ppl.12190. Manabe Y, Nafisi M, Verhertbruggen Y, et al. Loss-of-function mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall ACETYLATION and increased resistance to Botrytis cinerea. Plant Physiol. 2011;155(3):1068–78. https://doi.org/10.1104/pp.110.168989. Mortimer JC, Miles GP, Brown DM, et al. Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc Natl Acad Sci U S A. 2010;107:17409–14. https://doi.org/10.1073/pnas.1005456107. Orfila C, Sørensen SO, Harholt J, et al. QUASIMODO1 is expressed in vascular tissue of Arabidopsis thaliana inflorescence stems, and affects homogalacturonan and xylan biosynthesis. Planta. 2005;222(4):613–22. https://doi.org/10.1007/s00425-005-0008-z. Pauly M, Ramírez V. New insights into wall polysaccharide O-acetylation. Front Plant Sci. 2018;9:1210. https://doi.org/10.3389/fpls.2018.01210. Pawar PM, Ratke C, Balasubramanian VK, et al. Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification. New Phytol. 2017;214:1491–505. https://doi.org/10.1111/nph.14489. Peña MJ, Zhong R, Zhou GK, et al. Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell. 2007;19:549–63. https://doi.org/10.1105/tpc.106.049320. Rennie EA, Hansen SF, Baidoo EEK, et al. Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 2012;159:1408–17. https://doi.org/10.1104/pp.112.200964. Sado PE, Tessier D, Vasseur M, et al. Integrating genes and phenotype: a wheat–Arabidopsis–rice glycosyltransferase database for candidate gene analyses. Funct Integr Genomics. 2009;9(1):43–58. https://doi.org/10.1007/s10142-008-0100-0. Scheller HV, Ulvskov P. Hemicelluloses. Annu Rev Plant Biol. 2010;61:263–89. https://doi.org/10.1146/annurev-arplant-042809-112315. Schultink A, Naylor D, Dama M, et al. The role of the plant-specific ALTERED XYLOGLUCAN9 protein in Arabidopsis cell wall polysaccharide O-acetylation. Plant Physiol. 2015;167:1271–83. https://doi.org/10.1104/pp.114.256479. Urbanowicz BR, Peña MJ, Moniz HA, et al. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 2014;80(2):197–206. https://doi.org/10.1111/tpj.12643. Voxeur A, Andre A, Breton C, Lerouge P. Identification of putative Rhamnogalacturonan-II specific glycosyltransferases in Arabidopsis using a combination of bioinformatics approaches. PLoS One. 2012;7(12):e51129. https://doi.org/10.1371/journal.pone.0051129. Wierzbicki MP, Christie N, Pinard D, et al. A systems genetics analysis in Eucalyptus reveals coordination of metabolic pathways associated with xylan modification in wood-forming tissues. New Phytol. 2019;223:1952–72. https://doi.org/10.1111/nph.15972. Wu AM, Hörnblad E, Voxeur A, et al. Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol. 2010;153:542–54. https://doi.org/10.1104/pp.110.154971. Xu WL, Zhang DJ, Wu YF, et al. Cotton PRP5 gene encoding a proline-rich protein is involved in fiber development. Plant Mol Biol. 2013;82:353–65. https://doi.org/10.1007/s11103-013-0066-8. Zeng W, Lampugnani ER, Picard KL, et al. Asparagus IRX9, IRX10, and IRX14A are components of an active xylan backbone synthase complex that forms in the Golgi apparatus. Plant Physiol. 2016;171:93–109. https://doi.org/10.1104/pp.15.01919. Zhang T, Hu Y, Jiang W, et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM- 1) provides a resource for fiber improvement. Nat Biotechnol. 2015;33:531–7. https://doi.org/10.1038/nbt.3207. Zhong R, Cui D, Ye ZH. Regiospecific acetylation of xylan is mediated by a group of DUF231-containing O-acetyltransferases. Plant Cell Physiol. 2017;58:2126–38. https://doi.org/10.1093/pcp/pcx147. Zhong R, Peña MJ, Zhou GK, et al. Arabidopsis Fragile Fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell. 2005;17:3390–408. https://doi.org/10.1105/tpc.105.035501. Zhou GK, Zhong R, Himmelsbach DS, et al. Molecular characterization of PoGT8D and PoGT43B, two secondary wall-associated glycosyltransferases in poplar. Plant Cell Physiol. 2007;48(5):689–99. https://doi.org/10.1093/pcp/pcm037. Zhou GK, Zhong R, Richardson EA, et al. The poplar glycosyltransferase GT47C is functionally conserved with Arabidopsis Fragile Fiber8. Plant Cell Physiol. 2006;47(9):1229–40. https://doi.org/10.1093/pcp/pcj093.