AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (2.8 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper | Open Access

Brittle culm 25, which encodes an UDP-xylose synthase, affects cell wall properties in rice

Siliang Xua,1Mengchen Zhanga,1Junhua YeaDongxiu HuaYuanyuan ZhangaZhen LiaJunrong LiuaYanfei SunaShan WangaXiaoping YuanaYue FengaQun XuaXinghua Weia( )Dali Zengb( )Yaolong Yanga( )
China National Center for Rice Improvement/State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, Zhejiang, China
The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, Zhejiang A & F University, Hangzhou 311300, Zhejiang, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

Because plant mechanical strength influences plant growth and development, the regulatory mechanisms underlying cell-wall synthesis deserve investigation. Rice mutants are useful for such research. We have identified a novel brittle culm 25 (bc25) mutant with reduced growth and partial sterility. BC25 encodes an UDP-glucuronic acid decarboxylase involved in cellulose synthesis and belongs to the UXS family. A single-nucleotide mutation in BC25 accounts for its altered cell morphology and cell-wall composition. Transmission electron microscopy analysis showed that the thickness of the secondary cell wall was reduced in bc25. Monosaccharide analysis revealed significant increases in content of rhamnose and arabinose but not of other monosaccharides, indicating that BC25 was involved in xylose synthesis with some level of functional redundancy. Enzymatic assays suggested that BC25 functions with high activity to interconvert UDP-glucuronic acid (UDP-GlcA) and UDP-xylose. GUS staining showed that BC25 was ubiquitously expressed with higher expression in culm, root and sheath, in agreement with that shown by quantitative real-time (qRT)-PCR. RNA-seq further suggested that BC25 is involved in sugar metabolism. We conclude that BC25 strongly influences rice cell wall formation.

References

[1]

H. Chen, R. Fang, R. Deng, J. Li, The OsmiRNA166b-OsHox32 pair regulates mechanical strength of rice plants by modulating cell wall biosynthesis, Plant Biotechnol. J. 19 (2021) 1468-1480.

[2]

B. Zhang, Y. Gao, L. Zhang, Y. Zhou, The plant cell wall: biosynthesis, construction, and functions, J. Integr. Plant Biol. 63 (2021) 251-272.

[3]

Z. Hao, D. Mohnen, A review of xylan and lignin biosynthesis: foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes, Crit. Rev. Biochem. Mol. Biol. 49 (2014) 212-241.

[4]

C. Kesten, A. Menna, C. Sanchez-Rodriguez, Regulation of cellulose synthesis in response to stress, Curr. Opin. Plant Biol. 40 (2017) 106-113.

[5]

M. Mutwil, S. Debolt, S. Persson, Cellulose synthesis: a complex complex, Curr. Opin. Plant Biol. 11 (2008) 252-257.

[6]

J.R. Pear, Y. Kawagoe, W.E. Schreckengost, D.P. Delmer, D.M. Stalker, Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase, Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 12637-12642.

[7]

T. Kotake, T. Aohara, K. Hirano, A. Sato, Y. Kaneko, Y. Tsumuraya, H. Takatsuji, S. Kawasaki, Rice Brittle culm 6 encodes a dominant-negative form of CesA protein that perturbs cellulose synthesis in secondary cell walls, J. Exp. Bot. 62 (2011) 2053-2062.

[8]

F. Li, G. Xie, J. Huang, R. Zhang, Y.u. Li, M. Zhang, Y. Wang, A.o. Li, X. Li, T. Xia, C. Qu, F. Hu, A.J. Ragauskas, L. Peng, OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice, Plant Biotechnol. J. 15 (2017) 1093-1104.

[9]

S. Robert, G. Mouille, H. Hofte, The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose-deficient Arabidopsis mutants, Cellulose 11 (2004) 351-364.

[10]

N.G. Taylor, R.M. Howells, A.K. Huttly, K. Vickers, S.R. Turner, Interactions among three distinct CesA proteins essential for cellulose synthesis, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1450-1455.

[11]

K. Tanaka, K. Murata, M. Yamazaki, K. Onosato, A. Miyao, H. Hirochika, Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall, Plant Physiol. 133 (2003) 73-83.

[12]

C. Yan, S. Yan, X. Zeng, Z. Zhang, M. Gu, Fine mapping and isolation of Bc7(t), allelic to OsCesA4, J. Genet. Genomics 34 (2007) 1019-1027.

[13]

B. Zhang, L. Deng, Q. Qian, G. Xiong, D. Zeng, R. Li, L. Guo, J. Li, Y. Zhou, A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice, Plant Mol. Biol. 71 (2009) 509-524.

[14]

D. Wang, Y. Qin, J. Fang, S. Yuan, L. Peng, J. Zhao, X. Li, F. Chen, A missense mutation in the zinc finger domain of OsCESA7 deleteriously affects cellulose biosynthesis and plant growth in rice, PLoS ONE 11 (2016) e0153993.

[15]

Y.C. Rao, Y. Yang, D. Xin, X. Li, K. Zhai, B. Ma, J. Pan, Q. Qian, D. Zeng, Characterization and cloning of a brittle culm mutant (bc88) in rice (Oryza sativa L.), Chin. Sci. Bull. 58 (2013) 3000-3006.

[16]

X.Q. Song, L.F. Liu, Y.J. Jiang, B.C. Zhang, Y.P. Gao, X.L. Liu, Q.S. Lin, H.Q. Ling, Y.H. Zhou, Disruption of secondary wall cellulose biosynthesis alters cadmium translocation and tolerance in rice plants, Mol. Plant 6 (2013) 768-780.

[17]

J.E. Darvill, M. McNeil, A.G. Darvill, P. Albersheim, Structure of plant cell walls: XI. Glucuronoarabinoxylan, a second hemicellulose in the primary cell walls of suspension-cultured sycamore cells, Plant Physiol. 66 (1980) 1135-1139.

[18]

L. Zhang, C. Gao, F. Mentink-Vigier, L.U. Tang, D. Zhang, S. Wang, S. Cao, Z. Xu, X. Liu, T. Wang, Y. Zhou, B. Zhang, Arabinosyl deacetylase modulates the arabinoxylan acetylation profile and secondary wall formation, Plant Cell 31 (2019) 1113-1126.

[19]

E.A. Rennie, H.V. Scheller, Xylan biosynthesis, Curr. Opin. Biotechnol. 26 (2014) 100-107.

[20]

A. Ebringerova, T. Heinze, Xylan and xylan derivatives-biopolymers with valuable properties, 1-Naturally occurring xylans structures, procedures and properties, Macromol. Rapid Commun. 21 (2000) 542-556.

[21]

S. Gille, M. Pauly, O-acetylation of plant cell wall polysaccharides, Front. Plant Sci. 3 (2012) 12.

[22]

B. Zhang, L. Zhang, F. Li, D. Zhang, X. Liu, H. Wang, Z. Xu, C. Chu, Y. Zhou, Control of secondary cell wall patterning involves xylan deacetylation, Nat. Plants 3 (2017) 17017.

[23]

M. Pauly, S. Gille, L. Liu, N. Mansoori, A. de Souza, A. Schultink, G. Xiong, Hemicellulose biosynthesis, Planta 238 (2013) 627-642.

[24]

D.M. Brown, F. Goubet, W.W.A. Vicky, R. Goodacre, E. Stephens, P. Dupree, S.R. Turner, Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis, Plant J. 52 (2007) 1154-1168.

[25]

A.M. Wu, E. Hornblad, A. Voxeur, L. Gerber, C. Rihouey, P. Lerouge, A. Marchant, 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. 153 (2010) 542-554.

[26]

C. Lee, Q. Teng, W. Huang, R. Zhong, Z.H. Ye, The Arabidopsis family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone, Plant Physiol. 153 (2010) 526-541.

[27]

B.D. Keppler, A.M. Showalter, IRX14 and IRX14-LIKE, Two glycosyl transferases involved in glucuronoxylan biosynthesis and drought tolerance in Arabidopsis, Mol. Plant 3 (2010) 834-841.

[28]

H. Wang, H. Yang, Z. Wen, C. Gao, Y. Gao, Y. Tian, Z. Xu, X. Liu, S. Persson, B. Zhang, Y. Zhou, Xylan-based nanocompartments orchestrate plant vessel wall patterning, Nat. Plants 8 (2022) 295-306.

[29]

P. Dey, A. Roy, Molecular structure and catalytic mechanism of fungal family G acidophilic xylanases, 3 Biotech 8 (2018) 78.

[30]

T. Eixelsberger, S. Sykora, S. Egger, M. Brunsteiner, K.L. Kavanagh, U. Oppermann, L. Brecker, B. Nidetzky, Structure and mechanism of human UDP-xylose synthase, J. Biol. Chem. 287 (2012) 31349-31358.

[31]

M. Bar-Peled, C.L. Griffith, T.L. Doering, Functional cloning and characterization of a UDP-glucuronic acid decarboxylase: the pathogenic fungus Cryptococcus neoformans elucidates UDP-xylose synthesis, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 12003-12008.

[32]

B. Kuang, X. Zhao, C. Zhou, W. Zeng, J. Ren, B. Ebert, C.T. Beahan, X. Deng, Q. Zeng, G. Zhou, M.S. Doblin, J.L. Heazlewood, A. Bacic, X. Chen, A.M. Wu, Role of UDP-Glucuronic acid decarboxylase in xylan biosynthesis in Arabidopsis, Mol. Plant 9 (2016) 1119-1131.

[33]

B. Ebert, C. Rautengarten, X. Guo, G. Xiong, S. Stonebloom, A.M. Smith-Moritz, T. Herter, L.J.G. Chan, P.D. Adams, C.J. Petzold, M. Pauly, W.G.T. Willats, J.L. Heazlewood, H.V. Scheller, Identification and characterization of a golgi-localized UDP-xylose transporter family from Arabidopsis, Plant Cell 27 (2015) 1218-1227.

[34]

L. Guo, C. Chu, Q. Qian, Rice mutants and functional genomics, Chin. Bull. Bot. 23 (2006) 1-13.

[35]

D. Ren, Y. Rao, L. Huang, Y. Leng, J. Hu, M. Lu, G. Zhang, L. Zhu, Z. Gao, G. Dong, L. Guo, Q. Qian, D. Zeng, Fine mapping identifies a new QTL for brown rice rate in rice (Oryza Sativa L.), Rice 9 (2016) 4.

[36]

R. Tanaka, M. Hirashima, S. Satoh, A. Tanaka, The Arabidopsis-accelerated cell death Gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of the pheophorbide a oxygenase activity does not lead to the “stay-green” phenotype in Arabidopsis, Plant Cell Physiol. 44 (2003) 1266-1274.

[37]

M. Li, G. Xiong, R. Li, J. Cui, D. Tang, B. Zhang, M. Pauly, Z. Cheng, Y. Zhou, Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth, Plant J. 60 (2009) 1055-1069.

[38]
J.D. Thompson, T.J. Gibson, D.G. Higgins, Multiple sequence alignment using ClustalW and ClustalX, Curr. Protoc. Bioinf. 2 (2003) Unit 2.3.
[39]

S. Kumar, G. Stecher, M. Li, C. Knyaz, K. Tamura, MEGA X:molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol. 35 (2018) 1547-1549.

[40]

Y. Yang, J. Xu, L. Huang, Y. Leng, L. Dai, Y. Rao, L. Chen, Y. Wang, Z. Tu, J. Hu, D. Ren, G. Zhang, L.I. Zhu, L. Guo, Q. Qian, D. Zeng, PGL, encoding chlorophyllide a oxygenase 1, impacts leaf senescence and indirectly affects grain yield and quality in rice, J. Exp. Bot. 67 (2016) 1297-1310.

[41]

X. Zhao, K. Ouyang, S. Gan, W. Zeng, L. Song, S. Zhao, J. Li, M.S. Doblin, A. Bacic, X.Y. Chen, A. Marchant, X. Deng, A.M. Wu, Biochemical and molecular changes associated with heteroxylan biosynthesis in Neolamarckia cadamba (Rubiaceae) during xylogenesis, Front. Plant Sci. 5 (2014) 602.

[42]

A.F.N. Rosenberger, L. Hangelmann, A. Hofinger, I.B.H. Wilson, UDP-xylose and UDP-galactose synthesis in Trichomonas vaginalis, Mol. Biochem. Parasitol. 181 (2012) 53-56.

[43]

R.A. Jefferson, The GUS reporter gene system, Nature 342 (1989) 837-838.

[44]

S. Anders, P.T. Pyl, W. Huber, HTSeq-a Python framework to work with high-throughput sequencing data, Bioinformatics 31 (2015) 166-169.

[45]

Y. Cui, Y. Peng, Q. Zhang, S. Xia, B. Ruan, Q. Xu, X. Yu, T. Zhou, H.E. Liu, D. Zeng, G. Zhang, Z. Gao, J. Hu, L.i. Zhu, L. Shen, L. Guo, Q. Qian, D. Ren, Disruption of EARLY LESION LEAF 1, encoding a cytochrome P450 monooxygenase, induces ROS accumulation and cell death in rice, Plant J. 105 (2021) 942-956.

[46]

N. Ruan, Z. Dang, M. Wang, L. Cao, Y.E. Wang, S. Liu, Y. Tang, Y. Huang, Q. Zhang, Q. Xu, W. Chen, F. Li, J. Lunn, FRAGILE CULM 18 encodes a UDP-glucuronic acid decarboxylase required for xylan biosynthesis and plant growth in rice, J. Exp. Bot. 73 (2022) 2320-2335.

The Crop Journal
Pages 733-743
Cite this article:
Xu S, Zhang M, Ye J, et al. Brittle culm 25, which encodes an UDP-xylose synthase, affects cell wall properties in rice. The Crop Journal, 2023, 11(3): 733-743. https://doi.org/10.1016/j.cj.2022.11.011

318

Views

4

Downloads

10

Crossref

9

Web of Science

9

Scopus

0

CSCD

Altmetrics

Received: 09 June 2022
Revised: 31 October 2022
Accepted: 25 November 2022
Published: 02 January 2023
© 2022 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return