Characterization of a Novel Weak Allele of RGA1/D1 and Its Potential Application in Rice Breeding
Received date: 2022-01-27
Accepted date: 2022-03-28
Online published: 2022-08-29
Semi-dwarfing improves the lodging resistance and yield of rice, and the vast majority of modern rice varieties harbor the sd1 allele to decrease plant height, resulting in reduced genetic diversity and negative agronomic traits. Thus, exploring alternative sources of dwarfism is imperative for rice breeding. Here, we identified a novel RGA1 allele, d1-w, from a local indica variety Xiaolixiang (XLX) using a map-based cloning approach. Compared with other rice varieties, RGA1 in XLX contained a unique single nucleotide polymorphism that resulted in an additional transcript and reduced functional RGA1 transcript level. The RGA1 from Nipponbare was introduced into XLX to estimate the value of d1-w in rice breeding. Compared with transgenic XLX plants (XLXD1), XLX exhibited reduced plant height, increased stem strength, lower reactive oxygen species accumulation, delayed senescence, stronger photosynthesis, higher grain yield and quality (including external, milling and nutritional qualities), and enhanced resistance to drought and Rhizoctonia solani. Therefore, we proposed that the d1-w allele has potential as an excellent dwarfism resource for rice breeding.
Key words： rice; weak allele; RGA1; dwarf germplasm resource; yield; grain quality; drought resistance; sheath blight
Liu Yantong, Li Ting, Jiang Zhishu, Zeng Chuihai, He Rong, Qiu Jiao, Lin Xiaoli, Peng Limei, Song Yongping, Zhou Dahu, Cai Yicong, Zhu Changlan, Fu Junru, He Haohua, Xu Jie . Characterization of a Novel Weak Allele of RGA1/D1 and Its Potential Application in Rice Breeding[J]. Rice Science, 2022 , 29(6) : 522 -534 . DOI: 10.1016/j.rsci.2022.03.001
| [1] | Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S. 2012. The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science, 335: 1348-1351. |
| [2] | Asano K, Miyao A, Hirochika H, Kitano H, Matsuoka M, Ashikari M. 2010. SSD1, which encodes a plant-specific novel protein, controls plant elongation by regulating cell division in rice. Proc Jpn Acad Ser B Phys Biol Sci, 86(3): 265-273. |
| [3] | Asano K, Yamasaki M, Takuno S, Miura K, Katagiri S, Ito T, Doi K, Wu J Z, Ebana K, Matsumoto T, Innan H, Kitano H, Ashikari M, Matsuoka M. 2011. Artificial selection for a green revolution gene during japonica rice domestication. Proc Natl Acad Sci USA, 108(27): 11034-11039. |
| [4] | Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A. 1999. Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc Natl Acad Sci USA, 96(18): 10284-10289. |
| [5] | Assmann S M. 2005. G protein regulation of disease resistance during infection of rice with rice blast fungus. Sci STKE, 2005: cm13. |
| [6] | Caffarri S, Croce R, Cattivelli L, Bassi R. 2004. A look within LHCII: Differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry, 43(29): 9467-9476. |
| [7] | Chen W W, Cheng Z J, Liu L L, Wang M, You X M, Wang J, Zhang F, Zhou C L, Zhang Z, Zhang H, You S M, Wang Y P, Luo S, Zhang J H, Wang J L, Wang J, Zhao Z C, Guo X P, Lei C L, Zhang X, Lin Q B, Ren Y L, Zhu S S, Wan J M. 2019. Small Grain and Dwarf 2, encoding an HD-Zip II family transcription factor, regulates plant development by modulating gibberellin biosynthesis in rice. Plant Sci, 288: 110208. |
| [8] | Cui Y, Jiang N, Xu Z J, Xu Q. 2020. Heterotrimeric G protein are involved in the regulation of multiple agronomic traits and stress tolerance in rice. BMC Plant Biol, 20(1): 90. |
| [9] | Feng B H, Yang Y, Shi Y F, Lin L, Chen J, Wei Y L, Leung H, Wu J L. 2013. Genetic analysis and gene mapping of light brown spotted leaf mutant in rice. Rice Sci, 20(1): 13-18. |
| [10] | Ferrero-Serrano Á, Assmann S M. 2016. The α-subunit of the rice heterotrimeric G protein, RGA1, regulates drought tolerance during the vegetative phase in the dwarf rice mutant d1. J Exp Bot, 67(11): 3433-3443. |
| [11] | Ferrero-Serrano Á, Su Z, Assmann S M. 2018. Illuminating the role of the Gα heterotrimeric G protein subunit, RGA1, in regulating photoprotection and photoavoidance in rice. Plant Cell Environ, 41(2): 451-468. |
| [12] | Ferrero-Serrano Á, Cantos C, Assmann S M. 2019. The role of dwarfing traits in historical and modern agriculture with a focus on rice. Cold Spring Harb Perspect Biol, 11(11): a034645. |
| [13] | Fujisawa Y, Kato T, Ohki S, Ishikawa A, Kitano H, Sasaki T, Asahi T, Iwasaki Y. 1999. Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc Natl Acad Sci USA, 96(13): 7575-7580. |
| [14] | Gilman A G. 1987. G proteins: Transducers of receptor-generated signals. Annu Rev Biochem, 56: 615-649. |
| [15] | Hedden P. 2003. The genes of the green revolution. Trends Genet, 19(1): 5-9. |
| [16] | Hong Y B, Zhang Y X, Sinumporn S, Yu N, Zhan X D, Shen X H, Chen D B, Yu P, Wu W X, Liu Q E, Cao Z L, Zhao C D, Cheng S H, Cao L Y. 2018. Premature leaf senescence 3, encoding a methyltransferase, is required for melatonin biosynthesis in rice. Plant J, 95: 877-891. |
| [17] | Hong Z, Ueguchi-Tanaka M, Shimizu-Sato S, Inukai Y, Fujioka S, Shimada Y, Takatsuto S, Agetsuma M, Yoshida S, Watanabe Y, Uozu S, Kitano H, Ashikari M, Matsuoka M. 2002. Loss-of- function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. Plant J, 32(4): 495-508. |
| [18] | Hu J, Zhu L, Zeng D L, Gao Z Y, Guo L B, Fang Y X, Zhang G H, Dong G J, Yan M X, Liu J, Qian Q. 2010. Identification and characterization of NARROW AND ROLLED LEAF 1, a novel gene regulating leaf morphology and plant architecture in rice. Plant Mol Biol, 73(3): 283-292. |
| [19] | Khush G S. 2001. Green revolution: The way forward. Nat Rev Genet, 2(10): 815-822. |
| [20] | Li M R, Li H Q. 2003. A simple and highly efficient Agrobacterium- mediated rice transformation system. Acta Biol Exp Sin, 36(4): 289-294. (in Chinese with English abstract) |
| [21] | Li S, Tian Y H, Wu K, Ye Y F, Yu J P, Zhang J Q, Liu Q, Hu M Y, Li H, Tong Y P, Harberd N P, Fu X D. 2018. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature, 560: 595-600. |
| [22] | Liu C, Li L G. 2016. Advances in molecular understanding of rice lodging resistance. Chin J Rice Sci, 30(2): 216-222. (in Chinese with English abstract) |
| [23] | Liu F, Wang P D, Zhang X B, Li X F, Yan X H, Fu D H, Wu G. 2018. The genetic and molecular basis of crop height based on a rice model. Planta, 247(1): 1-26. |
| [24] | Liu X, Hu Q L, Yan J J, Sun K, Liang Y, Jia M R, Meng X B, Fang S, Wang Y Q, Jing Y H, Liu G F, Wu D X, Chu C C, Smith S M, Chu J F, Wang Y H, Li J Y, Wang B. 2020. ζ-carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Mol Plant, 13(12): 1784-1801. |
| [25] | Miura K, Agetsuma M, Kitano H, Yoshimura A, Matsuoka M, Jacobsen S E, Ashikari M. 2009. A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc Natl Acad Sci USA, 106(27): 11218-11223. |
| [26] | Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M S, Sato M, Nasu S, Minobe Y. 2002. Positional cloning of rice semidwarfing gene, sd-1: Rice ‘green revolution gene’ encodes a mutant enzyme involved in gibberellin synthesis. DNA Res, 9(1): 11-17. |
| [27] | Murai M, Hirose S, Sato S, Takebe M. 1991. Effects of dwarfing genes from dee-geo-woo-gen and other varieties on cool temperature tolerance at booting stage in rice. Jpn J Breed, 41(2): 241-254. |
| [28] | Murchie E H, Yang J C, Hubbart S, Horton P, Peng S B. 2002. Are there associations between grain-filling rate and photosynthesis in the flag leaves of field-grown rice? J Exp Bot, 53: 2217-2224. |
| [29] | Oki K, Inaba N, Kitagawa K, Fujioka S, Kitano H, Fujisawa Y, Kato H, Iwasaki Y. 2009. Function of the α subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol, 50: 161-172. |
| [30] | Pathak R R, Mandal V K, Jangam A P, Sharma N, Madan B, Jaiswal D K, Raghuram N. 2021. Heterotrimeric G-protein α subunit (RGA1) regulates tiller development, yield, cell wall, nitrogen response and biotic stress in rice. Sci Rep, 11: 2323. |
| [31] | Peng P, Gao Y D, Li Z, Yu Y W, Qin H, Guo Y, Huang R F, Wang J. 2019. Proteomic analysis of a rice mutant sd58 possessing a novel d1 allele of heterotrimeric G protein alpha subunit (RGA1) in salt stress with a focus on ROS scavenging. Int J Mol Sci, 20(1): 167. |
| [32] | Porra R J, Schäfer W, Cmiel E, Katheder I, Scheer H. 1994. The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. Eur J Biochem, 219(1/2): 671-679. |
| [33] | Qi W W, Sun F, Wang Q J, Chen M L, Huang Y Q, Feng Y Q, Luo X J, Yang J S. 2011. Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a gibberellin biosynthetic gene. Plant Physiol, 157(1): 216-228. |
| [34] | Sazuka T, Kamiya N, Nishimura T, Ohmae K, Sato Y, Imamura K, Nagato Y, Koshiba T, Nagamura Y, Ashikari M, Kitano H, Matsuoka M. 2009. A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. Plant J, 60(2): 227-241. |
| [35] | Sha H J, Liu H L, Zhao G X, Han Z M, Chang H L, Wang J G, Zheng H L, Zhang J F, Yu Y, Liu Y Q, Zou D T, Nie S J, Fang J. 2022. Elite sd1 alleles in japonica rice and their breeding applications in northeast China. Crop J, 10(1): 224-233. |
| [36] | Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K. 2002. The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA, 99(20): 13307-13312. |
| [37] | Sun H Y, Qian Q, Wu K, Luo J J, Wang S S, Zhang C W, Ma Y F, Liu Q, Huang X Z, Yuan Q B, Han R X, Zhao M, Dong G J, Guo L B, Zhu X D, Gou Z H, Wang W, Wu Y J, Lin H X, Fu X D. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet, 46(6): 652-656. |
| [38] | Sun Q, Yang S, Guo X F, Wang S T, Jia X T, Li S, Xuan Y H. 2021. RAVL1 activates IDD3 to negatively regulate rice resistance to sheath blight disease. Rice Sci, 28(2): 146-155. |
| [39] | Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M. 2000. Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA, 97(21): 11638-11643. |
| [40] | Urano D, Colaneri A, Jones A M. 2014. Gα modulates salt-induced cellular senescence and cell division in rice and maize. J Exp Bot, 65(22): 6553-6561. |
| [41] | Vikram P, Swamy B P M, Dixit S, Singh R, Singh B P, Miro B, Kohli A, Henry A, Singh N K, Kumar A. 2015. Drought susceptibility of modern rice varieties: An effect of linkage of drought tolerance with undesirable traits. Sci Rep, 5: 14799. |
| [42] | Wang F M, Yoshida H, Matsuoka M. 2021. Making the ‘green revolution’ truly green: Improving crop nitrogen use efficiency. Plant Cell Physiol, 62(6): 942-947. |
| [43] | Wang L, Xu Y Y, Ma Q B, Li D, Xu Z H, Chong K. 2006. Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. Cell Res, 16(12): 916-922. |
| [44] | Wang R N, Liu C, Li Q Z, Chen Z N, Sun S Y, Wang X L. 2020. Spatiotemporal resolved leaf angle establishment improves rice grain yield via controlling population density. iScience, 23(9): 101489. |
| [45] | Wang Z B, Zuo S M, Li G, Chen X J, Chen Z X, Zhang Y F, Pan X B. 2009. Rapid identification technology of resistance to rice sheath blight in seedling stage. Acta Phytopath Sin, 39: 174-182. (in Chinese with English abstract) |
| [46] | Yaish M W, El-Kereamy A, Zhu T, Beatty P H, Good A G, Bi Y M, Rothstein S J. 2010. The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet, 6(9): e1001098. |
| [47] | Yang Y L, Xu J, Huang L C, Leng Y J, Dai L P, Rao Y C, Chen L, Wang Y Q, Tu Z J, Hu J, Ren D Y, Zhang G H, Zhu L, Guo L B, Qian Q, Zeng D L. 2016. PGL, encoding chlorophyllide a oxygenase 1, impacts leaf senescence and indirectly affects grain yield and quality in rice. J Exp Bot, 67(5): 1297-1310. |
| [48] | Yuan L P. 2014. Development of hybrid rice to ensure food security. Rice Sci, 21(1): 1-2. |
| [49] | Zhu Y C, Li T, Xu J, Wang J J, Wang L, Zou W W, Zeng D L, Zhu L, Chen G, Hu J, Gao Z Y, Dong G J, Ren D Y, Shen L, Zhang Q, Guo L B, Hu S P, Qian Q, Zhang G H. 2020. Leaf width gene LW5/D1 affects plant architecture and yield in rice by regulating nitrogen utilization efficiency. Plant Physiol Biochem, 157: 359-369. |
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