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Bioinformatics studies on structures, functions and diversifications of rolling leaf related genes in rice (Oryza sativa L.)

Published online by Cambridge University Press:  11 November 2020

Md. Jahangir Alam Open the ORCID record for Md. Jahangir Alam [Opens in a new window] ,
Md. Alamin ,
Most. Humaira Sultana ,
Md. Asif Ahsan ,
Md. Ripter Hossain ,
S.M. Shahinul Islam  and
Md. Nurul Haque Mollah Open the ORCID record for Md. Nurul Haque Mollah [Opens in a new window]
Md. Jahangir Alam
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
Md. Alamin
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
Most. Humaira Sultana
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
Md. Asif Ahsan
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
Md. Ripter Hossain
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
S.M. Shahinul Islam
Affiliation:
Plant Biotechnology and Genetic Engineering Laboratory, Institute of Biological Sciences, University of Rajshahi, Rajshahi6205, Bangladesh
Md. Nurul Haque Mollah*
Affiliation:
Bioinformatics Laboratory, Department of Statistics, University of Rajshahi, Rajshahi6205, Bangladesh
*
*Corresponding author. E-mail: mollah.stat.bio@ru.ac.bd
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Abstract

Leaf morphology of crop plants has significant value in agronomy. Leaf rolling in rice plays a vital role to increase grain yield. However, collective information on the rolling leaf (RL) genes reported to date and different comparative bioinformatics studies of their sequences are still incomplete. This bioinformatics study was designed to investigate structures, functions and diversifications of the RL related genes reported till now through several studies. We performed different comparative and functional analyses of the selected 42 RL genes among 103 RL genes using different bioinformatics techniques including gene structure, conserved domain, phylogenetic, gene ontology (GO), transcription factor (TF), Kyoto Encyclopedia of Genes and Genomes (KEGG) and protein–protein network. Exon-intron organization and conserved domain analysis showed diversity in structures and conserved domains of RL genes. Phylogenetic analysis classified the proteins into five major groups. GO and TF analyses revealed that regulation-related genes were remarkably enriched in biological process and 10 different TF families were involved in rice leaf rolling. KEGG analysis demonstrated that 14 RL genes were involved in the KEGG pathways, among which 50% were involved in the metabolism pathways. Of the selected RL proteins, 55% proteins were non-interacting with other RL proteins and OsRL9 was the most interacting RL protein. These results provide important information regarding structures, conserved domains, phylogenetic revolution, protein–protein interactions and other genetic bases of RL genes which might be helpful to the researchers for functional analysis of new candidate RL genes to explore their characteristics and molecular mechanisms for high yield rice breeding.

Keywords

diversificationgene ontology and transcription factor analysisgene structure and functionKEGG pathway analysisphylogenetic analysisprotein–protein interaction networkricerolling leaf related genes
Type
Research Article
Information
Plant Genetic Resources , Volume 18 , Issue 5 , October 2020 , pp. 382 - 395
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of NIAB

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References

Alamin, M, Zeng, D-D, Qin, R, Sultana, MH, Jin, X-L and Shi, C-H (2017) Characterization and fine mapping of SFL1, a gene controlling Screw Flag Leaf in rice. Plant Molecular Biology Reporter 35: 491–503.CrossRefGoogle Scholar
Chen, Q, Xie, Q, Gao, J, Wang, W, Sun, B, Liu, B, Zhu, H, Peng, H, Zhao, H and Liu, C (2015) Characterization of Rolled and Erect Leaf 1 in regulating leave morphology in rice. Journal of Experimental Botany 66: 6047–6058.CrossRefGoogle ScholarPubMed
Chen, W, Wan, S, Shen, L, Zhou, Y, Huang, C, Chu, P and Guan, R (2018) Histological, physiological, and comparative proteomic analyses provide insights into leaf rolling in Brassica napus. Journal of Proteome Research 17: 1761–1772.CrossRefGoogle ScholarPubMed
Chen, W, Sheng, Z, Cai, Y, Li, Q, Wei, X, Xie, L, Jiao, G, Shao, G, Tang, S, Wang, J and Hu, P (2019) Rice Morphogenesis and Chlorophyll Accumulation Is Regulated by the Protein Encoded by NRL3 and Its Interaction With NAL9. Frontiers in Plant Science 10:175.CrossRefGoogle ScholarPubMed
Cho, SH, Yoo, SC, Zhang, H, Pandeya, D, Koh, HJ, Hwang, JY, Kim, GT and Paek, NC (2013) The rice narrow Leaf2 and narrow Leaf3 loci encode WUSCHEL-related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytologist 198: 1071–1084.CrossRefGoogle ScholarPubMed
Cho, S-H, Kang, K, Lee, S-H, Lee, I-J and Paek, N-C (2016) OsWOX3A is involved in negative feedback regulation of the gibberellic acid biosynthetic pathway in rice (Oryza sativa). Journal of Experimental Botany 67: 1677–1687.CrossRefGoogle Scholar
Cho, SH, Lee, CH, Gi, E, Yim, Y, Koh, HJ, Kang, K and Paek, NC (2018) The rice rolled fine striped (RFS) CHD3/Mi-2 chromatin remodeling factor epigenetically regulates genes involved in oxidative stress responses during leaf development. Frontiers in Plant Science 9: 364.CrossRefGoogle ScholarPubMed
Dai, M, Zhao, Y, Ma, Q, Hu, Y, Hedden, P, Zhang, Q and Zhou, DX (2007) The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiology 144: 121–133.CrossRefGoogle ScholarPubMed
Fang, L, Zhao, F, Cong, Y, Sang, X, Du, Q, Wang, D, Li, Y, Ling, Y, Yang, Z and He, G (2012) Rolling-leaf14 is a 2OG-Fe (II) oxygenase family protein that modulates rice leaf rolling by affecting secondary cell wall formation in leaves. Plant Biotechnology Journal 10: 524–532.CrossRefGoogle ScholarPubMed
Fujino, K, Matsuda, Y, Ozawa, K, Nishimura, T, Koshiba, T, Fraaije, MW and Sekiguchi, H (2008) NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Molecular Genetics and Genomics 279: 499–507.CrossRefGoogle ScholarPubMed
Hasan, MM, Basith, S, Khatun, MS, Lee, G, Manavalan, B and Kurata, H (2020a) Meta-i6mA: an interspecies predictor for identifying DNA N6-methyladenine sites of plant genomes by exploiting informative features in an integrative machine-learning framework. Briefings in Bioinformatics. https://doi.org/10.1093/bib/bbaa202CrossRefGoogle Scholar
Hasan, MM, Manavalan, B, Khatun, MS and Kurata, H (2020b) i4mC-ROSE, a bioinformatics tool for the identification of DNA N4-methylcytosine sites in the Rosaceae genome. International Journal of Biological Macromolecules 157: 752–758.CrossRefGoogle Scholar
Hasan, MM, Manavalan, B, Shoombuatong, W, Khatun, MS and Kurata, H (2020c) i4mC-Mouse: improved identification of DNA N4-methylcytosine sites in the mouse genome using multiple encoding schemes. Computational and Structural Biotechnology Journal 18: 906–912.CrossRefGoogle Scholar
Hasan, MM, Manavalan, B, Shoombuatong, W, Khatun, MS and Kurata, H (2020d) i6mA-Fuse: improved and robust prediction of DNA 6mA sites in the Rosaceae genome by fusing multiple feature representation. Plant Molecular Biology 103: 225–234.CrossRefGoogle Scholar
Hasan, MM, Schaduangrat, N, Basith, S, Lee, G, Shoombuatong, W and Manavalan, B (2020e) HLPpred-Fuse: improved and robust prediction of hemolytic peptide and its activity by fusing multiple feature representation. Bioinformatics (Oxford, England) 36: 3350–3356.CrossRefGoogle Scholar
Hibara, KI, Obara, M, Hayashida, E, Abe, M, Ishimaru, T, Satoh, H, Itoh, JI and Nagato, Y (2009) The ADAXIALIZED LEAF1 Gene functions in leaf and embryonic pattern formation in rice. Developmental Biology 334: 345–354.CrossRefGoogle ScholarPubMed
Hu, J, Zhu, L, Zeng, D, Gao, Z, Guo, L, Fang, Y, Zhang, G, Dong, G, Yan, M and Liu, J (2010) Identification and characterization of NARROW AND ROLLED LEAF 1, a novel gene regulating leaf morphology and plant architecture in rice. Plant Molecular Biology 73: 283–292.CrossRefGoogle ScholarPubMed
Hu, B, Jin, J, Guo, A-Y, Zhang, H, Luo, J and Gao, G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics (Oxford, England) 31: 1296–1297.CrossRefGoogle ScholarPubMed
Huang, J, Li, Z and Zhao, D (2016) Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Scientific Reports 6: 1–14.Google ScholarPubMed
Jin, J, Tian, F, Yang, D-C, Meng, Y-Q, Kong, L, Luo, J and Gao, G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research 45: D1040–D1045.CrossRefGoogle Scholar
Khatun, MS, Hasan, MM and Kurata, H (2019a) PreAIP: computational prediction of anti-inflammatory peptides by integrating multiple complementary features. Frontiers in Genetics 10: 129.CrossRefGoogle Scholar
Khatun, S, Hasan, M and Kurata, H (2019b) Efficient computational model for identification of antitubercular peptides by integrating amino acid patterns and properties. FEBS Letters 593: 3029–3039.CrossRefGoogle Scholar
Khush, GS (2013) Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breeding 132: 433–436.Google Scholar
Kirik, V and Bäumlein, H (1996) A novel leaf-specific myb-related protein with a single binding repeat. Gene 183: 109–113.CrossRefGoogle ScholarPubMed
Lang, Y, Zhang, Z, Gu, X, Yang, J and Zhu, Q (2004) Physiological and ecological effects of crimpy leaf character in rice (Oryza sativa L.) I. Leaf orientation, canopy structure and light distribution. Zuo Wu Xue Bao 30: 806–810.Google Scholar
Lee, YK, Woo, MO, Lee, D, Lee, G, Kim, B and Koh, HJ (2016) Identification of a novel candidate gene for rolled leaf in rice. Genes & Genomics 38: 1077–1084.CrossRefGoogle Scholar
Li, M, Xiong, G, Li, R, Cui, J, Tang, D, Zhang, B, Pauly, M, Cheng, Z and Zhou, Y (2009) Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth. The Plant Journal 60: 1055–1069.CrossRefGoogle ScholarPubMed
Li, L, Shi, ZY, Li, L, Shen, GZ, Wang, XQ, An, LS and Zhang, JL (2010) Overexpression of ACL1 (abaxially Curled Leaf 1) Increased bulliform cells and induced abaxial curling of leaf blades in rice. Molecular Plant 3: 807–817.CrossRefGoogle ScholarPubMed
Li, L, Xue, X, Zuo, SM, Chen, ZX, Zhang, YF, Li, QQ, Zhu, JK, Ma, YY, Pan, XB and Pan, CH (2013a) Suppressed expression of OsAGO1a leads to adaxial leaf rolling in rice. Chinese Journal of Rice Science 27: 223–230.Google Scholar
Li, W, Wu, C, Hu, G, Xing, L, Qian, W, Si, H, Sun, Z, Wang, X, Fu, Y and Liu, W (2013b) Characterization and fine mapping of a novel rice narrow leaf mutant nal9. Journal of Integrative Plant Biology 55: 1016–1025.CrossRefGoogle Scholar
Li, L, Xue, X, Chen, Z, Zhang, Y, Ma, Y, Pan, C, Zhu, J, Pan, X and Zuo, S (2014) Isolation and characterization of rl (t), a gene that controls leaf rolling in rice. Chinese Science Bulletin 59: 3142–3152.CrossRefGoogle Scholar
Li, C, Zou, X, Zhang, C, Shao, Q, Liu, J, Liu, B, Li, H and Zhao, T (2016) OsLBD3-7 Overexpression induced adaxially rolled leaves in rice. PLoS ONE 11: e0156413.CrossRefGoogle ScholarPubMed
Li, W-Q, Zhang, M-J, Gan, P-F, Qiao, L, Yang, S-Q, Miao, H, Wang, G-F, Zhang, M-M, Liu, W-T, Li, H-F, Shi, C-H and Chen, K-M (2017) CLD1/SRL1 modulates leaf rolling by affecting cell wall formation, epidermis integrity and water homeostasis in rice. The Plant Journal 92: 904–923.CrossRefGoogle ScholarPubMed
Liang, R, Qin, R, Zeng, DD, Zheng, X, Jin, XL and Shi, CH (2016) Phenotype analysis and gene mapping of narrow and rolling leaf mutant nrl4 in rice (Oryza sativa L.). Scientia Agricultura Sinica 49: 3863–3873.Google Scholar
Liu, B, Li, P, Li, X, Liu, C, Cao, S, Chu, C and Cao, X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiology 139: 296–305.CrossRefGoogle ScholarPubMed
Liu, C, Kong, WY, You, SM, Zhong, XJ, Jiang, L, Zhao, ZG and Wan, JM (2015) Genetic analysis and fine mapping of a novel rolled leaf gene in rice. Scientia Agricultura Sinica 48: 2487–2496.Google Scholar
Liu, X, Li, M, Liu, K, Tang, D, Sun, M, Li, Y, Shen, Y, Du, G and Cheng, Z (2016) Semi-Rolled Leaf2 modulates rice leaf rolling by regulating abaxial side cell differentiation. Journal of Experimental Botany 67: 2139–2150.CrossRefGoogle ScholarPubMed
Ma, Y, Wang, F, Guo, J and Zhang, XS (2009) Rice OsAS2 gene, a member of LOB domain family, functions in the regulation of shoot differentiation and leaf development. Journal of Plant Biology 52: 374–381.CrossRefGoogle Scholar
Ma, Y, Zhao, Y, Shangguan, X, Shi, S, Zeng, Y, Wu, Y, Chen, R, You, A, Zhu, L, Du, B and He, G (2017) Overexpression of OsRRK1 changes leaf morphology and defense to insect in rice. Frontiers in Plant Science 8: 1–14.CrossRefGoogle ScholarPubMed
Marchler-Bauer, A and Bryant, SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Research 32: W327–W331.CrossRefGoogle ScholarPubMed
Marchler-Bauer, A, Lu, S, Anderson, JB, Chitsaz, F, Derbyshire, MK, DeWeese-Scott, C, Fong, JH, Geer, LY, Geer, RC, Gonzales, NR, Gwadz, M, Hurwitz, DI, Jackson, JD, Ke, Z, Lanczycki, CJ, Lu, F, Marchler, GH, Mullokandov, M, Omelchenko, MV, Robertson, CL, Song, JS, Thanki, N, Yamashita, RA, Zhang, D, Zhang, N, Zheng, C and Bryant, SH (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Research 39: D225–D229.CrossRefGoogle ScholarPubMed
Marchler-Bauer, A, Derbyshire, MK, Gonzales, NR, Lu, S, Chitsaz, F, Geer, LY, Geer, RC, He, J, Gwadz, M, Hurwitz, DI, Lanczycki, CJ, Lu, F, Marchler, GH, Song, JS, Thanki, N, Wang, Z, Yamashita, RA, Zhang, D, Zheng, C and Bryant, SH (2015) CDD: NCBI's conserved domain database. Nucleic Acids Research 43: D222–D226.CrossRefGoogle ScholarPubMed
Mosharaf, MP, Hassan, MM, Ahmed, FF, Khatun, MS, Moni, MA and Mollah, MNH (2020) Computational prediction of protein ubiquitination sites mapping on Arabidopsis thaliana. Computational Biology and Chemistry 85: 107238.CrossRefGoogle ScholarPubMed
Nuruzzaman, M, Manimekalai, R, Sharoni, AM, Satoh, K, Kondoh, H, Ooka, H and Kikuchi, S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465: 30–44.CrossRefGoogle ScholarPubMed
Qi, J, Qian, Q, Bu, Q, Li, S, Chen, Q, Sun, J, Liang, W, Zhou, Y, Chu, C and Li, X (2008) Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiology 147: 1947–1959.CrossRefGoogle ScholarPubMed
Rahman, H, Yang, J, Xu, Y-P, Munyampundu, J-P and Cai, X-Z (2016) Phylogeny of plant CAMTAs and role of AtCAMTAs in nonhost resistance to Xanthomonas oryzae pv. oryzae. Frontiers in Plant Science 7: 177.CrossRefGoogle ScholarPubMed
Schauer, N and Fernie, AR (2006) Plant metabolomics: towards biological function and mechanism. Trends in Plant Science 11: 508–516.CrossRefGoogle ScholarPubMed
Segami, S, Kono, I, Ando, T, Yano, M, Kitano, H, Miura, K and Iwasaki, Y (2012) Small and Round Seed 5 Gene encodes alpha-tubulin regulating seed cell elongation in rice. Rice 5: 4.CrossRefGoogle ScholarPubMed
Shen, NW (2011) Genetic analysis and gene mapping for the semi-curled leaf mutant in rice (Oryza sativa L.). Beijing: Graduate School of Chinese Academy of Agricultural Sciences 9: 1002–1013.Google Scholar
Shi, Z, Wang, J, Wan, X, Shen, G, Wang, X and Zhang, J (2007) Over-expression of rice OsAGO7 gene induces upward curling of the leaf blade that enhanced erect-leaf habit. Planta 226: 99–108.CrossRefGoogle ScholarPubMed
Shi, L, Wei, X, Adedze, Y, Sheng, Z, Tang, S, Hu, P and Wang, J (2016) Characterization and gene cloning of the rice (Oryza sativa L.) dwarf and narrow-leaf mutant dnl3. Genetics and Molecular Research 15: gmr8731.CrossRefGoogle ScholarPubMed
Szklarczyk, D, Morris, JH, Cook, H, Kuhn, M, Wyder, S, Simonovic, M, Santos, A, Doncheva, NT, Roth, A, Bork, P, Jensen, LJ and Mering, CV (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Research 45: D362–D368.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.CrossRefGoogle ScholarPubMed
Toriba, T, Harada, K, Takamura, A, Nakamura, H, Ichikawa, H, Suzaki, T and Hirano, H-Y (2007) Molecular characterization the YABBY Gene family in Oryza sativa and expression analysis of OsYABBY1. Molecular Genetics and Genomics 277: 457–468.CrossRefGoogle ScholarPubMed
Wang, L, Xu, J, Nian, J, Shen, N, Lai, K, Hu, J, Zeng, D, Ge, C, Fang, Y, Zhu, L, Qian, Q and Zhang, G (2016) Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regulation 78: 345–356.CrossRefGoogle Scholar
Wang, X, Wang, F, Chen, H, Liang, X, Huang, Y and Yi, J (2017) Comparative genomic hybridization and transcriptome sequencing reveal that two genes, OsI_14279 (LOC_Os03g62620) and OsI_10794 (LOC_Os03g14950) regulate the mutation in the γ-rl rice mutant. Physiology and Molecular Biology of Plants 23: 745–754.CrossRefGoogle ScholarPubMed
Woo, Y-M, Park, H-J, Su'udi, M, Yang, J-I, Park, J-J, Back, K, Park, Y-M and An, G (2007) Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Molecular Biology 65: 125–136.CrossRefGoogle Scholar
Wu, X (2009) Prospects of developing hybrid rice with super high yield. Agronomy Journal 101: 688–695.CrossRefGoogle Scholar
Wu, C, Fu, Y, Hu, G, Si, H, Cheng, S and Liu, W (2010) Isolation and characterization of a rice mutant with narrow and rolled leaves. Planta 232: 313–324.CrossRefGoogle ScholarPubMed
Wu, R, Li, S, He, S, Waßmann, F, Yu, C, Qin, G, Schreiber, L, Qu, L-J and Gu, H (2011) CFL1, A WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. The Plant Cell 23: 3392–3411.CrossRefGoogle ScholarPubMed
Wu, Y, Luo, L, Chen, L, Tao, X, Huang, M, Wang, H, Chen, Z and Xiao, W (2016) Chromosome mapping, molecular cloning and expression analysis of a novel gene response for leaf width in rice. Biochemical and Biophysical Research Communications 480: 394–401.CrossRefGoogle ScholarPubMed
Xia, ML, Tang, DY, Yang, YZ, Li, YX, Wang, WW, Lu, H, Liu, XM and Lin, JZ (2017) Preliminary study on the rice OsYABBY6 gene involving in the regulation of leaf development. Life Science Research 21: 23–30.Google Scholar
Xiang, JJ, Zhang, GH, Qian, Q and Xue, HW (2012) SEMI-ROLLED LEAF1 Encodes a putative glycosylphosphatidylinositol-anchored protein and modulates rice leaf rolling by regulating the formation of bulliform cells. Plant Physiology 159: 1488–1500.CrossRefGoogle ScholarPubMed
Xu, Y, Wang, Y, Long, Q, Huang, J, Wang, Y, Zhou, K, Zheng, M, Sun, J, Chen, H and Chen, S (2014) Overexpression of OsZHD1, a zinc finger homeodomain class homeobox transcription factor, induces abaxially curled and drooping leaf in rice. Planta 239: 803–816.CrossRefGoogle ScholarPubMed
Yan, S, Yan, C-J, Zeng, X-H, Yang, Y-C, Fang, Y-W, Tian, C-Y, Sun, Y-W, Cheng, Z-K and Gu, M-H (2008) ROLLED LEAF 9, Encoding a GARP protein, regulates the leaf abaxial cell fate in rice. Plant Molecular Biology 68: 239–250.CrossRefGoogle ScholarPubMed
Yang, C, Li, D, Liu, X, Ji, C, Hao, L, Zhao, X, Li, X, Chen, C, Cheng, Z and Zhu, L (2014) OsMYB103L, an R2R3-MYB transcription factor, influences leaf rolling and mechanical strength in rice (Oryza sativa L.). BMC Plant Biology 14: 158.CrossRefGoogle Scholar
Yang, SQ, Li, WQ, Miao, H, Gan, PF, Qiao, L, Chang, YL, Shi, CH and Chen, KM (2016) REL2, A gene encoding an unknown function protein which contains DUF630 and DUF632 domains controls leaf rolling in rice. Rice 9: 37.CrossRefGoogle ScholarPubMed
Ye, Y, Wu, K, Chen, J, Liu, Q, Wu, Y, Liu, B and Fu, X (2018) OsSND2, a NAC family transcription factor, is involved in secondary cell wall biosynthesis through regulating MYBs expression in rice. Rice 11: 36.CrossRefGoogle ScholarPubMed
Yoshimura, A, Ideta, O and Iwata, N (1997) Linkage map of phenotype and RFLP markers in rice. Plant Molecular Biology 35: 49–60.CrossRefGoogle ScholarPubMed
Yoshizawa, AC, Itoh, M, Okuda, S, Moriya, Y and Kanehisa, M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35: W182–W185.Google Scholar
Yuan, L (1997) Hybrid rice breeding for super high yield. Hybrid Rice 12: 1–6.Google Scholar
Zhang, G-H, Xu, Q, Zhu, X-D, Qian, Q and Xue, H-W (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. The Plant Cell 21: 719–735.CrossRefGoogle ScholarPubMed
Zhang, X, Rerksiri, W, Liu, A, Zhou, X, Xiong, H, Xiang, J, Chen, X and Xiong, X (2013) Transcriptome profile reveals heat response mechanism at molecular and metabolic levels in rice flag leaf. Gene 530: 185–192.CrossRefGoogle ScholarPubMed
Zhang, JJ, Wu, SY, Jiang, L, Wang, JL, Zhang, X, Guo, XP, Wu, CY and Wan, JM (2015) A detailed analysis of the leaf rolling mutant sll2 reveals complex nature in regulation of bulliform cell development in rice (Oryza sativa L.). Plant Biology 17: 437–448.CrossRefGoogle Scholar
Zhang, J, Zhang, H, Srivastava, AK, Pan, Y, Bai, J, Fang, J, Shi, H and Zhu, JK (2018) Knock-down of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiology 176: 2082–2094.CrossRefGoogle Scholar
Zhou, K, Ma, Y, Liu, T, Shen, M and Pan, S (1995) The breeding of subspecific heavy ear hybrid rice-exploration about super-high yield breeding of hybrid rice. Journal of Sichuan Agricultural University 13: 403–407.Google Scholar
Zhao, SQ, Hu, J, Guo, LB, Qian, Q and Xue, HW (2010) Rice leaf inclination2, a VIN3-like protein, regulates leaf angle through modulating cell division of the collar. Cell Research 20: 935–947.CrossRefGoogle ScholarPubMed
Zhao, J, Luo, H, Jiang, Y, Yang, X and Zha, R (2017) Gene mapping for rice narrow leaf mutant Narrow Leaf 11 (nal11). Journal of Southern Agriculture 48: 1133–1138.Google Scholar
Zhou, Y, Wang, D, Wu, T, Yang, Y, Liu, C, Yan, L, Tang, D, Zhao, X, Zhu, Y and Lin, J (2018) LRRK1, A receptor-like cytoplasmic kinase, regulates leaf rolling through modulating bulliform cell development in rice. Molecular Breeding 38: 48.CrossRefGoogle Scholar
Zou, LP, Sun, XH, Zhang, ZG, Liu, P, Wu, JX, Tian, CJ, Qiu, JL and Lu, TG (2011) Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiology 156: 1589–1602.CrossRefGoogle ScholarPubMed
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