Mutations in the microRNA172 binding site of SUPERNUMERARY BRACT (SNB) suppress internode elongation in rice
Tóm tắt
Internode elongation is an important agronomic trait in rice that determines culm length, which is related to lodging, panicle exsertion, and biomass. sui4 (shortened uppermost internode 4) mutants show reduced internode length and a dwarf phenotype due to shortened internodes; the uppermost internode is particularly severely affected. The present study was performed to identify the molecular nature and function of the SUI4 gene during internode elongation. Our previous study showed that the SUI4 gene was mapped to a 1.1-Mb interval on chromosome 7 (Ji et al. 2014). In order to isolate the gene responsible for the sui4 phenotype, genomic DNA resequencing of sui4 mutants and wild-type plants and reciprocal transformation of wild-type and mutant alleles of the putative SUI4 gene was performed. The data revealed that the causative mutation of sui4 was a T to A nucleotide substitution at the microRNA172 binding site of Os07g0235800, and that SUI4 is a new allele of the previously reported gene SUPERNUMERARY BRACT (SNB), which affects flower structure. In order to understand the effect of this mutation on expression of the SUI4/SNB gene, SUI4/SNB native promoter-fuzed GUS transgenics were examined, along with qRT-PCR analysis at various developmental stages. In sui4 mutants, the SUI4/SNB gene was upregulated in the leaves, culms, and panicles, especially when internodes were elongated. In culms, SUI4/SNB was expressed in the nodes and the lower parts of elongating internodes. In order to further explore the molecular nature of SUI4/SNB during internode elongation, RNA-seq and qRT-PCR analysis were performed with RNAs from the culms of sui4 mutants and wild-type plants in the booting stage. The data showed that in sui4 mutants, genes deactivating bioactive gibberellins and cytokinin were upregulated while genes related to cell expansion and cell wall synthesis were downregulated. In summary, this paper shows that interaction between SUI4/SNB and microRNA172 could determine internode elongation during the reproductive stage in rice plants. Due to a mutation at the microRNA172 binding site in sui4 mutants, the expression of SUI4/SNB was enhanced, which lowered the activities of cell expansion and cell wall synthesis and consequently resulted in shortened internodes.
Tài liệu tham khảo
Aya K, Hobo T, Sato-Izawa K, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) A novel AP2-type transcription factor, SMALL ORGAN SIZE1, controls organ SIZE downstream of an auxin signaling pathway. Plant Cell Physiol 55(5):897–912. https://doi.org/10.1093/pcp/pcu023
Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, Feldmann KA (1999) The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11(2):207–221
Chonan N (1993) Chapter 3. Stem. In: Matsuo T, Hoshikawa K (eds) Science of the Rice Plant, vol 1. Nobunkyo, Tokyo, pp 187–188
Dai Z, Gao J, An K, Lee JM, Edwards GE, An G (1996) Promoter elements controlling developmental and environmental regulation of a tobacco ribosomal protein gene L34. Plant Mol Biol 32(6):1055–1065
Dinh TT, Girke T, Liu X, Yant L, Schmid M, Chen X (2012) The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139:1978–1986. https://doi.org/10.1242/dev.077073
Frankova L, Fry SC (2013) Biochemistry and physiological roles of enzymes that 'cut and paste' plant cell-wall polysaccharides. J Exp Bot 64(12):3519–3550. https://doi.org/10.1093/jxb/ert201
Huang D, Wang S, Zhang B, Shang-Guan K, Shi Y, Zhang D, Liu X, Wu K, Xu Z, Fu X, Zhou Y (2015) A gibberellin-mediated DELLA-NAC signaling Cascade regulates cellulose synthesis in Rice. Plant Cell 27(6):1681–1696. https://doi.org/10.1105/tpc.15.00015
Huang DW, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, Lempicki RA (2007) DAVID bioinformatics resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic acids res 35(web server issue):W169-175. https://doi.org/10.1093/nar/gkm415
Imamura T, Kusano H, Kajigaya Y, Ichikawa M, Shimada H (2007) A rice dihydrosphingosine C4 hydroxylase (DSH1) gene, which is abundantly expressed in the stigmas, vascular cells and apical meristem, may be involved in fertility. Plant Cell Physiol 48(8):1108–1120. https://doi.org/10.1093/pcp/pcm084
Ito Y, Kimura F, Hirakata K, Tsuda K, Takasugi T, Eiguchi M, Nakagawa K, Kurata N (2011) Fatty acid elongase is required for shoot development in rice. Plant J 66(4):680–688. https://doi.org/10.1111/j.1365-313X.2011.04530.x
Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46(1):23–47
Je BI, Piao HL, Park SJ, Park SH, Kim CM, Xuan YH, Park SH, Huang J, Do Choi Y, An G, Wong HL, Fujioka S, Kim MC, Shimamoto K, Han CD (2010) RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 22(6):1777–1791
Ji H, Kim H, Yun D-W, Yoon U-H, Kim T-H, Eun M-Y, Lee G-S (2014) Characterization and fine mapping of a shortened uppermost internode mutant in rice. Plant biotechnology reports 8:125-134. Doi. https://doi.org/10.1007/s11816-013-0280-5
Kende H, van der Knaap E, Cho HT (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118(4):1105–1110
Lee DY, An G (2012) Two AP2 family genes, supernumerary bract (SNB) and Osindeterminate spikelet 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J 69(3):445–461. https://doi.org/10.1111/j.1365-313X.2011.04804.x
Lee DY, Lee J, Moon S, Park SY, An G (2007) The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J 49(1):64–78. https://doi.org/10.1111/j.1365-313X.2006.02941.x
Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38(9):3081–3093. https://doi.org/10.1093/nar/gkp1240
Lee YS, Lee DY, Cho LH, An G (2014) Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice (N Y) 7(1):31. https://doi.org/10.1186/s12284-014-0031-4
Li Y, Jones L, McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6(6):603–610
Liu F, Wang P, Zhang X, Li X, Yan X, Fu D, Wu G (2018) The genetic and molecular basis of crop height based on a rice model. Planta 247(1):1–26. https://doi.org/10.1007/s00425-017-2798-1
Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JA, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20(10):2603–2618. https://doi.org/10.1105/tpc.108.060913
Park HL, Bhoo SH, Kwon M, Lee SW, Cho MH (2017) Biochemical and expression analyses of the Rice Cinnamoyl-CoA reductase gene family. Front Plant Sci 8:2099. https://doi.org/10.3389/fpls.2017.02099
Swetha C, Basu D, Pachamuthu K, Tirumalai V, Nair A, Prasad M, Shivaprasad PV (2018) Major domestication-related phenotypes in Indica Rice are due to loss of miRNA-mediated laccase silencing. Plant Cell 30(11):2649–2662. https://doi.org/10.1105/tpc.18.00472
Teotia S, Tang G (2015) To bloom or not to bloom: role of microRNAs in plant flowering. Mol Plant 8(3):359–377. https://doi.org/10.1016/j.molp.2014.12.018
Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26(11):4376–4393. https://doi.org/10.1105/tpc.114.132092
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111. https://doi.org/10.1093/bioinformatics/btp120
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515. https://doi.org/10.1038/nbt.1621
Wang L, Yin H, Qian Q, Yang J, Huang C, Hu X, Luo D (2009) NECK LEAF 1, a GATA type transcription factor, modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice. Cell Res 19(5):598–611
Wang W, Li G, Zhao J, Chu H, Lin W, Zhang D, Wang Z, Liang W (2014) Dwarf Tiller1, a Wuschel-related homeobox transcription factor, is required for tiller growth in rice. PLoS Genet 10(3):e1004154. https://doi.org/10.1371/journal.pgen.1004154
Yaish MW, El-Kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet 6(9):e1001098. https://doi.org/10.1371/journal.pgen.1001098
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12(9):1591–1606
Zhang LY, Bai MY, Wu J, Zhu JY, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, Yang H, Xu Y, Kim SH, Fujioka S, Lin WH, Chong K, Lu T, Wang ZY (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21(12):3767–3780. https://doi.org/10.1105/tpc.109.070441
Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62(2):487–495. https://doi.org/10.1093/jxb/erq295
Zhu QH, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol 9:149. https://doi.org/10.1186/1471-2229-9-149