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Research Article | Open Access

OsPEX1, a leucine-rich repeat extensin protein, functions in the regulation of caryopsis development and quality in rice

Xin Luana,c,1, Shanwen Kea,1, Shuchun Liua,1, Guojian Tanga, Dahui Huangb, Minyi Weib, Yuexiong Zhangb, Gang Qinb( ), Xiang-Qian Zhanga,c( )
Guangdong Engineering Research Center of Grassland Science, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, Guangdong, China
Rice Research Institute, Guangxi Academy of Agricultural Sciences/Guangxi Key Laboratory of Rice Genetics and Breeding, Nanning 530007, Guangxi, China
Guangdong Laboratory of Lingnan Modern Agricultural Science and Technology, Guangzhou 510642, Guangdong, China

1 These authors contributed equally to this work.

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Abstract

Rice caryopses are enclosed by outer glumes. The size and dimension of the outer glume are the main determinants of caryopsis size. However, it is unclear whether caryopsis development is completely dependent on the size of the glume, or whether it can grow and expand autonomously despite the constraint of glume enclosure. We report the identification of a mutant line that produces normal-sized glumes with smaller mature caryopses that do not fill the entire glume cavity. The caryopsis phenotype in the pex1 mutant is caused by a reduction in cell size. OsPEX1, a leucine-rich repeat extensin gene, was highly expressed in the developing caryopsis. Overexpression of OsPEX1 driven by a constitutive promoter recapitulated the mutant phenotype, showing that the small-caryopsis phenotype is caused by overexpression of the OsPEX1 gene. Free amino acids, including several essential amino acids, and crude protein were increased in pex1 relative to the wild type, endowing pex1 with improved nutritional quality. Our results suggest that caryopsis development can be genetically uncoupled from maternally controlled glume development and that OsPEX1 might be a new resource for improving nutritional quality of rice cultivars.

Keywords

Grain sizeRiceCaryopsisGlumeExtensin-like protein

References

[1]

H. Yoshida, Y. Nagato, Flower development in rice, J. Exp. Bot. 62 (2011) 4719-4730.
Crossref Google Scholar
[2]

R. Huang, L. Jiang, J. Zheng, T. Wang, H. Wang, Y. Huang, Z. Hong, Genetic bases of rice grain shape: so many genes, so little known, Trends Plant Sci. 18 (2013) 218-226.
Crossref Google Scholar
[3]

N.A. Li, R. Xu, Y. Li, Molecular networks of seed size control in plants, Annu. Rev. Plant Biol. 70 (2019) 435-463.
Crossref Google Scholar
[4]

D. Heang, H. Sassa, K. Wu, Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice, PLoS ONE 7 (2012), e31325.
Crossref Google Scholar
[5]

Y. Abe, K. Mieda, T. Ando, I. Kono, M. Yano, H. Kitano, Y. Iwasaki, The SMALL AND ROUND SEED1 (SRS1/DEP2) gene is involved in the regulation of seed size in rice, Genes Genet. Syst. 85 (2010) 327-339.
Crossref Google Scholar
[6]

K. Kitagawa, S. Kurinami, K. Oki, Y. Abe, T. Ando, I. Kono, M. Yano, H. Kitano, Y. Iwasaki, A novel kinesin 13 protein regulating rice seed length, Plant Cell Physiol. 51 (2010) 1315-1329.
Crossref Google Scholar
[7]

J. Luo, H. Liu, T. Zhou, B. Gu, X. Huang, Y. Shangguan, J. Zhu, Y. Li, Y. Zhao, Y. Wang, Q. Zhao, A. Wang, Z. Wang, T. Sang, Z. Wang, B. Han, An-1 Encodes a basic helix-loop-helix protein that regulates awn development, grain size, and grain number in rice, Plant Cell 25 (2013) 3360-3376.
Crossref Google Scholar
[8]

P. Qi, Y.S. Lin, X.J. Song, J.B. Shen, W. Huang, J.X. Shan, M.Z. Zhu, L. Jiang, J.P. Gao, H.X. Lin, The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3, Cell Res. 22 (2012) 1666-1680.
Crossref Google Scholar
[9]

S. Segami, I. Kono, T. Ando, M. Yano, H. Kitano, K. Miura, Y. Iwasaki, Small and round seed 5 gene encodes alpha-tubulin regulating seed cell elongation in rice, Rice 5 (2012) 4.
Crossref Google Scholar
[10]

X. Zhang, J. Wang, J. Huang, H. Lan, C. Wang, C. Yin, Y. Wu, H. Tang, Q. Qian, J. Li, H. Zhang, Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 21534-21539.
Crossref Google Scholar
[11]

H. Nakagawa, A. Tanaka, T. Tanabata, M. Ohtake, S. Fujioka, H. Nakamura, H. Ichikawa, M. Mori, SHORT GRAIN1 decreases organ elongation and brassinosteroid response in rice, Plant Physiol. 158 (2012) 1208-1219.
Crossref Google Scholar
[12]

C. Yamamuro, Y. Ihara, X. Wu, T. Noguchi, S. Fujioka, S. Takatsuto, M. Ashikari, H. Kitano, M. Matsuoka, Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint, Plant Cell 12 (2000) 1591-1605.
Crossref Google Scholar
[13]

M. Mori, T. Nomura, H. Ooka, M. Ishizaka, T. Yokota, K. Sugimoto, K. Okabe, H. Kajiwara, K. Satoh, K. Yamamoto, H. Hirochika, S. Kikuchi, Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis, Plant Physiol. 130 (2002) 1152-1161.
Crossref Google Scholar
[14]

Z. Hong, M. Ueguchi-Tanaka, K. Umemura, S. Uozu, S. Fujioka, S. Takatsuto, S. Yoshida, M. Ashikari, H. Kitano, M. Matsuoka, A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450, Plant Cell 15 (2003) 2900-2910.
Crossref Google Scholar
[15]

S. Tanabe, M. Ashikari, S. Fujioka, S. Takatsuto, S. Yoshida, M. Yano, A. Yoshimura, H. Kitano, M. Matsuoka, Y. Fujisawa, H. Kato, Y. Iwasaki, A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length, Plant Cell 17 (2005) 776-790.
Crossref Google Scholar
[16]

X. Zhang, J. Sun, X. Cao, X. Song, Epigenetic mutation of RAV6 affects leaf angle and seed size in rice, Plant Physiol. 169 (2015) 2118-2128.
Crossref Google Scholar
[17]

K. Oki, N. Inaba, K. Kitagawa, S. Fujioka, H. Kitano, Y. Fujisawa, H. Kato, Y. Iwasaki, Function of the α subunit of rice heterotrimeric G protein in brassinosteroid signaling, Plant Cell Physiol. 50 (2009) 161-172.
Crossref Google Scholar
[18]

M. Ashikari, J. Wu, M. Yano, T. Sasaki, A. Yoshimura, Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 10284-10289.
Crossref Google Scholar
[19]

K. Oki, N. Inaba, H. Kitano, S. Takahashi, Y. Fujisawa, H. Kato, Y. Iwasaki, Study of novel d1 alleles, defective mutants of the alpha subunit of heterotrimeric G-protein in rice, Genes Genet. Syst. 84 (1) (2009) 35-42.
Crossref Google Scholar
[20]

C.L. Shi, N.Q. Dong, T. Guo, W.W. Ye, J.X. Shan, H.X. Lin, A quantitative trait locus GW6 controls rice grain size and yield through the gibberellin pathway, Plant J. 103 (2020) 1174-1188.
Crossref Google Scholar
[21]

R. Xu, P. Duan, H. Yu, Z. Zhou, B. Zhang, R. Wang, J. Li, G. Zhang, S. Zhuang, J. Lyu, N. a. Li, T. Chai, Z. Tian, S. Yao, Y. Li, Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice, Mol. Plant 11 (2018) 860-873.
Crossref Google Scholar
[22]

Z.Y. Deng, L.T. Liu, T. Li, S. Yan, B.J. Kuang, S.J. Huang, C.J. Yan, T. Wang, OsKinesin-13A is an active microtubule depolymerase involved in glume length regulation via affecting cell elongation, Sci. Rep. 5 (2015) 9457.
Crossref Google Scholar
[23]

X. Liu, R. Wolfe, L.R. Welch, D.S. Domozych, Z.A. Popper, A.M. Showalter, O.A. Zabotina, Bioinformatic identification and analysis of extensins in the plant kingdom, PLoS ONE 11 (2016), e0150177.
Crossref Google Scholar
[24]

N. Baumberger, M. Steiner, U. Ryser, B. Keller, C. Ringli, Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development, Plant J. 35 (2003) 71-81.
Crossref Google Scholar
[25]

N. Baumberger, C. Ringli, B. Keller, The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana, Genes Dev. 15 (2001) 1128-1139.
Crossref Google Scholar
[26]

C. Draeger, T.N. Fabrice, E. Gineau, G. Mouille, B.M. Kuhn, I. Moller, M.T. Abdou, B. Frey, M. Pauly, A. Bacic, C. Ringli, Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth, BMC Plant Biol. 15 (2015) 155.
Crossref Google Scholar
[27]

F. Liu, X. Zhang, Z. Zhang, Z. Chen, H. Zhu, J. Wang, J. Zhang, G. Zhang, Transpositional behaviour of the Ds element in the Ac/Ds system in rice, Chin. Sci. Bull. 52 (2007) 2789-2796.
Crossref Google Scholar
[28]

S. Ke, X. Luan, J. Liang, Y.H. Hung, T.F. Hsieh, X.Q. Zhang, Rice OsPEX1, an extensin-like protein, affects lignin biosynthesis and plant growth, Plant Mol. Biol. 100 (2019) 151-161.
Crossref Google Scholar
[29]

Y.L. Han, H.X. Song, Q. Liao, Y. Yu, S.F. Jian, J.E. Lepo, Q. Liu, X.M. Rong, C. Tian, J. Zeng, C.Y. Guan, A.M. Ismail, Z.H. Zhang, Nitrogen use efficiency is mediated by vacuolar nitrate sequestration capacity in roots of Brassica napus, Plant Physiol. 170 (2016) 1684-1698.
Crossref Google Scholar
[30]

V. Šimat, I. Hamed, S. Petričević, T. Bogdanović, Seasonal changes in free amino acid and fatty acid compositions of sardines, Sardina pilchardus (Walbaum, 1792): implications for nutrition, Foods 9 (2020) 867.
Crossref Google Scholar
[31]

B. Teng, R. Zeng, Y. Wang, Z. Liu, Z. Zhang, H. Zhu, X. Ding, W. Li, G. Zhang, Detection of allelic variation at the Wx locus with single-segment substitution lines in rice (Oryza sativa L.), Mol. Breed. 30 (2012) 583-595.
Crossref Google Scholar
[32]

G. Lu, X. Li, S. Ding, Quick analysis of starch content of sweetpotato by HCl hydrolysis-DNS method, J. Chin. Cereals Oils Assoc. 1 (2002) 25-28 (in Chinese with English abstract).
Google Scholar
[33]

B. Teng, Y. Zhang, J. Wu, X. Cong, R. Wang, Y. Han, Z. Luo, Association between allelic variation at the Waxy locus and starch physicochemical properties using single-segment substitution lines in rice, Starch 65 (2013) 1069-1077.
Crossref Google Scholar
[34]

Y.F. Tan, J.X. Li, S.B. Yu, Y.Z. Xing, C.G. Xu, Q. Zhang, The three important traits for cooking and eating quality of rice grains are controlled by a single locus in an elite rice hybrid, Shanyou 63, Theor. Appl. Genet. 99 (1999) 642-648.
Crossref Google Scholar
[35]

N. Baumberger, B. Doesseger, R. Guyot, A. Diet, R.L. Parsons, M.A. Clark, M.P. Simmons, P. Bedinger, S.A. Goff, C. Ringli, B. Keller, Whole-genome comparison of leucine-rich repeat extensins in Arabidopsis and rice, a conserved family of cell wall proteins form a vegetative and a reproductive clade, Plant Physiol. 131 (2003) 1313-1326.
Crossref Google Scholar
[36]

A. Herger, K. Dünser, J. Kleine-Vehn, C. Ringli, Leucine-rich repeat extensin proteins and their role in cell wall sensing, Curr. Biol. 29 (2019) R851-R858.
Crossref Google Scholar
[37]

S. Moussu, C. Broyart, G. Santos-Fernandez, S. Augustin, S. Wehrle, U. Grossniklaus, J. Santiago, Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth, Proc. Natl. Acad. Sci. U. S. A. 117 (2020) 7494-7503.
Crossref Google Scholar
[38]

K. Takeda, K. Ichinohe, K.I. Saito, Mechanism of grain notching, and variation for notched grain frequency in rice, Jpn. J. Crop Sci. 50 (1981) 502-508.
Crossref Google Scholar
[39]

Z. Xiong, S. Min, F. Kong, X. Zhu, Genetic analysis of notched grain in rice, Chin. J. Rice. Sci. 1 (1986) 26-34 (in Chinese with English abstract).
Google Scholar
[40]

K.U. Torii, N. Mitsukawa, T. Oosumi, Y. Matsuura, R. Yokoyama, R.F. Whittier, Y. Komeda, The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats, Plant Cell 8 (1996) 735-746.
Crossref Google Scholar
[41]

W.Y. Song, G.L. Wang, L.L. Chen, H.S. Kim, L.Y. Pi, T. Holsten, J. Gardner, B. Wang, W.X. Zhai, L.H. Zhu, C. Fauquet, P. Ronald, A Receptor kinase-like protein encoded by the rice disease resistance gene, Xa21, Science 270 (1995) 1804-1806.
Crossref Google Scholar
[42]

T.L. Jinn, J.M. Stone, J.C. Walker, HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission, Genes Dev. 14 (2000) 108-117.
Crossref Google Scholar
[43]

Q. i. Hall, M.C. Cannon, The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis, Plant Cell 14 (2002) 1161-1172.
Crossref Google Scholar
[44]

N.C. Carpita, D.M. Gibeaut, Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth, Plant J. 3 (1993) 1-30.
Crossref Google Scholar
[45]

C.S. Ahn, H.K. Ahn, H.S. Pai, Overexpression of the PP2A regulatory subunit Tap46 leads to enhanced plant growth through stimulation of the TOR signalling pathway, J. Exp. Bot. 66 (3) (2015) 827-840.
Crossref Google Scholar
[46]

N. Dong, Y. Sun, T. Guo, C. Shi, Y. Zhang, Y. Kan, Y. Xiang, H. Zhang, Y. Yang, Y. Li, H. Zhao, H. Yu, Z. Lu, Y. Wang, W. Ye, J. Shan, H. Lin, UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice, Nat. Commun. 11 (2020) 2629.
Crossref Google Scholar
[47]

S. Zhao, L. Zhao, F. Liu, Y. Wu, Z. Zhu, C. Sun, L. Tan, NARROW AND ROLLED LEAF 2 regulates leaf shape, male fertility, and seed size in rice, J. Integr. Plant Biol. 58 (2016) 983-996.
Crossref Google Scholar
[48]

K.S. Nissen, W.G.T. Willats, F.G. Malinovsky, Understanding CrRLK1L function: cell walls and growth control, Trends Plant Sci. 21 (2016) 516-527.
Crossref Google Scholar
[49]

Y. u. Xiao, M. Stegmann, Z. Han, T.A. DeFalco, K. Parys, L. i. Xu, Y. Belkhadir, C. Zipfel, J. Chai, Mechanisms of RALF peptide perception by a heterotypic receptor complex, Nature 572 (2019) 270-274.
Crossref Google Scholar
[50]

G. Xu, W. Chen, L. Song, Q. Chen, H. Zhang, H. Liao, G. Zhao, F. Lin, H. Zhou, F. Yu, C. Foyer, FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in response to the carbon/nitrogen ratio, J. Exp. Bot. 70 (2019) 6375-6388.
Crossref Google Scholar
[51]

S. Zhu, J.M. Estévez, H. Liao, Y. Zhu, T. Yang, C. Li, Y. Wang, L. Li, X. Liu, J.M. Pacheco, H. Guo, F. Yu, The RALF1-FERONIA complex phosphorylates eIF4E1 to promote protein synthesis and polar root hair growth, Mol. Plant 13 (2020) 698-716.
Crossref Google Scholar
[52]

T. Yang, L. Wang, C. Li, Y. Liu, S. Zhu, Y. Qi, X. Liu, Q. Lin, S. Luan, F. Yu, Receptor protein kinase FERONIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase, Biochem. Bioph. Res. Commu. 465 (2015) 77-82.
Crossref Google Scholar
[53]

L. Wang, D. Wang, Z. Yang, S. Jiang, J. Qu, W. He, Z. Liu, J. Xing, Y. Ma, Q. Lin, F. Yu, Roles of FERONIA-like receptor genes in regulating grain size and quality in rice, Sci. China Life Sci. 64 (2021) 294-310.
Crossref Google Scholar
[54]

S. Zhu, Q. Fu, F. Xu, H. Zheng, F. Yu, New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signaling network, New Phytol. 1168–1183 (2021).
Crossref Google Scholar
[55]

C. Borassi, A.R. Sede, M.A. Mecchia, J.D. Salgado Salter, E. Marzol, J.P. Muschietti, J.M. Estevez, An update on cell surface proteins containing extensin-motifs, J. Exp. Bot. 67 (2016) 477-487.
Crossref Google Scholar
[56]

B.D. Kohorn, S.L. Kohorn, The cell wall-associated kinases, WAKs, as pectin receptors, Front. Plant Sci. 3 (2012) 88.
Crossref Google Scholar
[57]

M.A. Mecchia, G. Santos-Fernandez, N.N. Duss, S.C. Somoza, A. Boisson-Dernier, V. Gagliardini, A. Martínez-Bernardini, T.N. Fabrice, C. Ringli, J.P. Muschietti, U. Grossniklaus, RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis, Science 358 (2017) 1600-1603.
Crossref Google Scholar
The Crop Journal
Volume 10 Issue 3,
June 2022
Pages 704-715
DOI: 10.1016/j.cj.2021.10.001
Cite this article:
Luan X, Ke S, Liu S, et al. OsPEX1, a leucine-rich repeat extensin protein, functions in the regulation of caryopsis development and quality in rice. The Crop Journal, 2022, 10(3): 704-715. https://doi.org/10.1016/j.cj.2021.10.001

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Received: 29 April 2021
Revised: 16 September 2021
Accepted: 16 October 2021
Published: 29 November 2021
© 2021 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/).
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