Dissection of Genetic Mechanism of Abnormal Heading in Hybrid Rice

doi:DOI: 10.1016/S1672-6308(13)60184-5

Abstract

Abstract:

Abnormal heading in hybrid rice production has caused great economic loss in recent years, but the genetic basis of this phenomenon remains elusive. In this study, we developed four testcross populations using 38 introgression lines (ILs) from Shuhui 527 (SH527)/Fuhui 838 (FH838)//SH527 population as male parents and four male sterile lines (MSLs; namely II-32A, Xieqingzao A, Gang 46A and Jin 23A) as female parents. Progeny testing allowed us to identify 55 abnormal heading combinations in Hefei, but had late heading date in Hangzhou and Guangzhou of China. By one- and two-way analysis of variance, a total of 21 QTLs and 31 pairs of epistatic QTLs associated with photosensitivity were identified in the four populations, respectively. Genotypic analysis showed that the IL parent of most abnormal heading combinations showed some introgressions at markers RM331 and RM3395 on chromosome 8 (strongly associated with the known genes OsHAP3H/DTH8/Ghd8/LHD1) of donor FH838 alleles, and these two markers were also identified as affecting photosensitivity. The observation that the recipient parent (SH527), donor parent (FH838), their testcross combinations with four MSLs, and the IL parents of abnormal heading combinations had normal heading date in Hefei suggested that OsHAP3H/DTH8/Ghd8/LHD1 showed no independent regulation on abnormal heading in the abnormal heading combinations. It is noteworthy that complex epistasis among RM331 or RM3395 with other loci, including dominant × additive, additive × dominant, and dominant × dominant epistases, were identified only in the four testcross populations of the current study, but not in the SH527/FH838//SH527 population, suggesting the cause of abnormal heading in abnormal heading combinations in Hefei and delayed heading in Hangzhou and Guangzhou.

Key words: hybrid rice, abnormal heading, photosensitivity, QTL mapping, genetic mechanism

ZHANG Hong-jun, QU Li-jun, XIANG Chao, WANG Hui, XIA Jia-fa, LI Ze-fu, GAO Yong-ming, SHI Ying-yao. Dissection of Genetic Mechanism of Abnormal Heading in Hybrid Rice[J]. RICE SCIENCE, DOI: DOI: 10.1016/S1672-6308(13)60184-5 .

References

Bai H S, Wang B H. 1991. Analysis of the reason on abnormal heading in hybrid rice and control strategy. Seed World, 9: 35. (in Chinese)
Cheng S H, Zhuang J Y, Fan Y Y, Du J H, Cao L Y. 2007. Progress in research and development on hybrid rice: A super-domesticate in China. Ann Bot, 100(5): 959–966.
College of Nanjing. 1979. Crop Cultivation. Shanghai: Shaihai Science and Technology Publisher: 34–35. (in Chinese)
Dai C, Xue H W. 2010. Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signaling. EMBO J, 29(11): 1916–1927.
Dai J. 2011. Studies on construction of SSR fingerprints among parental lines in hybrid rice (Oryza sativa L.) and identification of two-line hybrids and Daqingke [PhD thesis]. Nanjing: Nanjing Agricultural University: 19–20. (in Chinese)
Dai X D, Ding Y N, Tan L B, Fu Y C, Liu F X, Zhu Z F, Sun X Y, Sun X W, Gu P, Cai H W, Sun C Q. 2012. LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J Integr Plant Biol, 54(10): 790–799.
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A. 2004. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Gene Dev, 18(8): 926–936.
Hayama R, Izawa T, Shimamoto K. 2002. Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. Plant Cell Physiol, 43(5): 494–504.
Hu S K, Su Y, Ye W J, Guo L B. 2012. Advances in genetic analysis and molecular regulation mechanism of heading date in rice (Oryza sativa L.). Chin J Rice Sci, 26(3): 373–382. (in Chinese with English abstract)
Izawa T, Oikawa T, Tokutomi S, Okuno K, Shimanoto K. 2000. Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). Plant J, 22(5): 391–399.
Kim S K, Yun C H, Lee J H, Jang Y H, Park H Y, Kim J K. 2008. OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like gene sunder SD conditions in rice. Planta, 228: 355–365.
Kim S L, Lee S, Kim H J, Nam H G, An G. 2007. OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol, 145(4): 1484–1494.
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M. 2002. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol, 43(10): 1096–1105.
Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimanoto K. 2008. Hd3a and RFT1 are essential for flowering in rice. Development, 135(4): 767–774.
Lee S, Kim J, Han J J, Han M J, An G. 2004. Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/ AGL20) ortholog in rice. Plant J, 38(5): 754–764.
Li D J, Yang C H, Li X B, Gan Q, Zhao X F, Zhu L H. 2009. Functional characterization of rice OsDof12. Planta, 229(6): 1159–1169.
Li K P, Kang Y Q, Lu C P. 2010. Growth characteristics and control measures of abnormal heading in hybrid rice field. Seed, 29(3): 123–125. (in Chinese)
Matsubara K, Yamanouchi U, Wang Z X, Minobe Y, Izawa T, Yano M. 2008. Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol, 148(3): 1425–1435.
Lim J, Moon Y H, An G, Jang S K. 2000. Two rice MADS domain proteins interact with OsMADS1. Plant Mol Biol, 44(5): 513–527.
Lu Z M, Ma C Y. 1987. Impurity and control measures for hybrid rice. Seed, 27: 38–39. (in Chinese)
Ryu C H, Lee S, Cho L H, Kim S L, Lee Y S, Choi S C, Jeong H J, Yi J, Park S J, Han C D, An G. 2009. OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ, 32(10): 1412–1427.
Shinozuka Y, Kojima S, Shomura A, Ichimura H, Yano M, Yamamoto K, Sasaki T. 1999. Isolation and characterization of rice MADS box gene homologues and their RFLP mapping. DNA Res, 6(2): 123–129.
Takahashi Y, Shomura A, Sasaki T, Yano M. 2001. Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA, 98(14): 7922–7927.
Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N. 2008. Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genom, 279(3): 279–289.
Thomson M J, Tai T H, McClung A M, Lai X H, Hinga M E, Lobos K B, Xu Y, Martinez C P, McCouch S R. 2003. Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet, 107: 479–493.
Wei X J, Xu J F, Guo H N, Jiang L, Chen S H, Yu C Y, Zhou Z L, Hu P S, Zhai H Q, Wan J M. 2010. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol, 153(4): 1747–1758.
Xue W Y, Xing Y Z, Weng X Y, Zhao Y, Tang W J, Wang L, Zhou H J, Yu S B, Xu C G, Li X H, Zhang Q F. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet, 40: 761–767.
Yan W H, Wang P, Chen H X, Zhou H J, Li Q P, Wang C R, Ding Z H, Zhang Y S, Yu S B, Xing Y Z, Zhang Q F. 2011. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant, 4(2): 319–330.
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell, 12(12): 2473–2483.
Yu Z W. 2003. Selective Crop Cultivation. Beijing: China Agriculture Press: 154–155. (in Chinese)
Yuan L P. 1986. Hybrid rice in China. Chin J Rice Sci, 1: 8–18. (in Chinese with English abstract)
Zhang H J, Wang H, Qian Y L, Xia J F, Li Z F, Shi Y Y, Zhu L H, Ali J, Gao Y M, Li Z K. 2013. Simultaneous improvement and genetic dissection of grain yield and its related traits in a backbone parent of hybrid rice (Oryza sativa L.) using selective introgression. Mol Breeding, 31(1): 181–194.
Zhou Y, Cui G K, Zhang Y Z, Guan C R, Chang S Y, Gu M H, Liang G H. 2012. Fine mapping of a major QTL qHd8.1 for heading date in rice. Chin J Rice Sci, 26(1): 43–48. (in Chinese with English abstract)
Zuo J R, Li J Y. 2014. Molecular dissection of complex agronomic traits of rice: A team effort by Chinese scientists in recent years. Natl Sci Rev, 1(2): 253–276.

[1]	LI Qianlong, FENG Qi, WANG Heqin, KANG Yunhai, ZHANG Conghe, DU Ming, ZHANG Yunhu, WANG Hui, CHEN Jinjie, HAN Bin, FANG Yu, WANG Ahong. Genome-Wide Dissection of Quan 9311A Breeding Process and Application Advantages [J]. Rice Science, 2023, 30(6): 7-.
[2]	Lu Xuedan, Li Fan, Xiao Yunhua, Wang Feng, Zhang Guilian, Deng Huabing, Tang Wenbang. Grain Shape Genes: Shaping the Future of Rice Breeding [J]. Rice Science, 2023, 30(5): 379-404.
[3]	Ngangkham Umakanta, Kumar Parida Swarup, Kumar Singh Ashok, Mohapatra Trilochan. Differential RNA Editing of Mitochondrial Genes in WA-Cytoplasmic Based Male Sterile Line Pusa 6A, and Its Maintainer and Restorer Lines [J]. Rice Science, 2019, 26(5): 282-289.
[4]	Khlaimongkhon Sudthana, Chakhonkaen Sriprapai, Pitngam Keasinee, Ditthab Khanittha, Sangarwut Numphet, Panyawut Natjaree, Wasinanon Thiwawan, Mongkolsiriwatana Chareerat, Chunwongse Julapark, Muangprom Amorntip. Molecular Markers and Candidate Genes for Thermo-Sensitive Genic Male Sterile in Rice [J]. Rice Science, 2019, 26(3): 147-156.
[5]	Hong-guang Xie, Jia-huang Jiang, Yan-mei Zheng, Yong-sheng Zhu, Fang-xi Wu, Xi Luo, Qiu-hua Cai, Jian-fu Zhang, Hua-an Xie. Development of Hybrid Rice Variety FY7206 with Blast Resistance Gene Pid3 and Cold Tolerance Gene Ctb1 [J]. Rice Science, 2016, 23(5): 266-273.
[6]	Guan-fu Fu, Cai-xia Zhang, Yong-jie Yang, Jie Xiong, Xue-qin Yang, Xiu-fu Zhang, Qian-yu Jin, Long-xing Tao. Male Parent Plays More Important Role in Heat Tolerance in Three-Line Hybrid Rice [J]. Rice Science, 2015, 22(3): 116-122.
[7]	Zhi-yuan Huang, Bing-ran Zhao, Qi-ming Lv, Xi-qin Fu, Ye-yun Xin, Long-ping Yuan. Heterosis Expression of Hybrid Rice in Natural- and Short-Day Length Conditions [J]. Rice Science, 2015, 22(2): 81-88.
[8]	J. Arasakesary S., Manonmani S., Pushpam R., Robin S.. New Temperature Sensitive Genic Male Sterile Lines with Better Outcrossing Ability for Production of Two-Line Hybrid Rice [J]. Rice Science, 2015, 22(1): 49-52.
[9]	LIANG Yan, ZHANG Xue-mei, LI De-qiang, HUANG Fu, HU Pei-song, PENG Yun-liang. Integrated Approach to Control False Smut in Hybrid Rice in Sichuan Province, China [J]. RICE SCIENCE, 2014, 21(6): 354-360.
[10]	Mohammad H. FOTOKIAN, Kayvan AGAHI. Biplot Analysis of Genotype by Environment for Cooking Quality in Hybrid Rice: A Tool for Line × Tester Data [J]. RICE SCIENCE, 2014, 21(5): 282-287.
[11]	LU Yong-liang, Nilda R. BURGOS, WANG Wei-xia, YU Liu-qing. Transgene Flow from Glufosinate-Resistant Rice to Improved and Weedy Rice in China [J]. RICE SCIENCE, 2014, 21(5): 271-281.
[12]	TANEE Sreewongchai, WEERACHAI Matthayatthaworn, CHALERMPOL Phumichai, PRAPA Sripichitt. Introgression of Gene for Non-Pollen Type Thermo-Sensitive Genic Male Sterility to Thai Rice Cultivars [J]. RICE SCIENCE, 2014, 21(2): 123-126.
[13]	LUO Li-li1, 2, #, ZHANG Ying-xin1, #, CHEN Dai-bo1, ZHAN Xiao-deng1, SHEN Xi-hong1, CHENG Shi-hua1, CAO Li-yong1. QTL Mapping for Hull Thickness and Related Traits in Hybrid Rice Xieyou 9308 [J]. RICE SCIENCE, 2014, 21(1): 29-38.
[14]	YUAN Long-ping. Development of Hybrid Rice to Ensure Food Security [J]. RICE SCIENCE, 2014, 21(1): 1-2.
[15]	TIAN Fu-kuan1, 2, #, RUAN Ban-pu1, 3, #, YAN Mei-xian1, YE Shi-fang1, PENG You-lin1, DONG Guo-jun1, ZHU Li1, HU Jiang1, YAN Hong-lan1, GUO Long-biao1, QIAN Qian1, GAO Zhen-yu1. Genetic Analysis and QTL Mapping of Mature Seed Culturability in Indica Rice [J]. RICE SCIENCE, 2013, 20(5): 313-319.