Journal of Genetics and Genomics

Understanding the genetic and molecular constitutions of heterosis for developing hybrid rice

Yidan Ouyang, Xu Li, Qifa Zhang

2022, 49(5): 385-393. doi: 10.1016/j.jgg.2022.02.022

Abstract (399) PDF (76)

Abstract:
The wide adoption of hybrid rice has greatly increased rice yield in the last several decades. The utilization of heterosis facilitated by male sterility has been a common strategy for hybrid rice development. Here, we summarize our efforts in the genetic and molecular understanding of heterosis and male sterility together with the related progress from other research groups. Analyses of F₁ diallel crosses show that strong heterosis widely exists in hybrids of diverse germplasms, and inter-subspecific hybrids often display higher heterosis. Using the elite hybrid Shanyou 63 as a model, an immortalized F₂ population design is conducted for systematic characterization of the biological mechanism of heterosis, with identification of loci controlling heterosis of yield and yield component traits. Dominance, overdominance, and epistasis all play important roles in the genetic basis of heterosis; quantitative assessment of these components well addressed the three classical genetic hypotheses for heterosis. Environment-sensitive genic male sterility (EGMS) enables the development of two-line hybrids, and long noncoding RNAs often function as regulators of EGMS. Inter-subspecific hybrids show greatly reduced fertility; the identification and molecular characterization of hybrid sterility genes offer strategies for overcoming inter-subspecific hybrid sterility. These developments have significant implications for future hybrid rice improvement using genomic breeding.

Nitrogen assimilation in plants: current status and future prospects

Xiujie Liu, Bin Hu, Chengcai Chu

2022, 49(5): 394-404. doi: 10.1016/j.jgg.2021.12.006

Abstract (833) PDF (148)

Abstract:
Nitrogen (N) is the driving force for crop yields; however, excessive N application in agriculture not only increases production cost, but also causes severe environmental problems. Therefore, comprehensively understanding the molecular mechanisms of N use efficiency (NUE) and breeding crops with higher NUE is essential to tackle these problems. NUE of crops is determined by N uptake, transport, assimilation, and remobilization. In the process of N assimilation, nitrate reductase (NR), nitrite reductase (NiR), glutamine synthetase (GS), and glutamine-2-oxoglutarate aminotransferase (GOGAT, also known as glutamate synthase) are the major enzymes. NR and NiR mediate the initiation of inorganic N utilization, and GS/GOGAT cycle converts inorganic N to organic N, playing a vital role in N assimilation and the final NUE of crops. Besides, asparagine synthetase (ASN), glutamate dehydrogenase (GDH), and carbamoyl phosphate synthetase (CPSase) are also involved. In this review, we summarize the function and regulation of these enzymes reported in three major crops—rice, maize, and wheat, also in the model plant Arabidopsis, and we highlight their application in improving NUE of crops via manipulating N assimilation. Anticipated challenges and prospects toward fully understanding the function of N assimilation and further exploring the potential for NUE improvement are discussed.

Natural variations in grain length 10 (GL10) regulate rice grain size

Penglin Zhan, Shuaipeng Ma, Zhili Xiao, Fangping Li, Xin Wei, Shaojun Lin, Xiaoling Wang, Zhe Ji, Yu Fu, Jiahao Pan, Mi Zhou, Yue Liu, Zengyuan Chang, Lu Li, Suhong Bu, Zupei Liu, Haitao Zhu, Guifu Liu, Guiquan Zhang, Shaokui Wang

2022, 49(5): 405-413. doi: 10.1016/j.jgg.2022.01.008

Abstract (634) PDF (143)

Abstract:
Grain size is an important determinant of grain weight and yield in rice. Although several genes related to grain size have been identified, natural variations in these genes that affect grain size are poorly characterized. Here, we describe the grain length QTL GL10, encoding MADS56, which positively regulates grain length and grain weight. A natural allelic variation of NIL-gl10, containing an ~1.0-kb deletion in the first exon that abolishes its transcription, results in shorter grain length, lower grain weight and delayed flowering in gl10 plants. The knockout of GL10 in the HJX74 background leads to grain phenotypes similar to that of NIL-gl10, while overexpression of GL10 results in increased grain length and weight and earlier heading date. GL10 regulates grain length by promoting greater longitudinal cell growth in the grain glume. Additionally, GL10 participates in the regulation of gibberellic acid (GA) signaling pathway genes in young panicle tissues. Analysis of GL10 haplotypes shows obvious divergence between the japonica and indica lineages. Our findings reveal an allelic variation of GL10 that may explain differences in grain length among modern cultivars and could be used to breed rice varieties with optimized grain shape.

OsbZIP60-mediated unfolded protein response regulates grain chalkiness in rice

Weiping Yang, Pengkun Xu, Juncheng Zhang, Shuo Zhang, Zhenwei Li, Ke Yang, Xinyuan Chang, Yibo Li

2022, 49(5): 414-426. doi: 10.1016/j.jgg.2022.02.002

Abstract (408) PDF (98)

Abstract:
Grain chalkiness, an undesirable trait caused by complex factors, has great negative impacts on the quality and economic value of rice. However, little is known about the regulatory mechanism of grain chalkiness, particularly the effect of endoplasmic reticulum (ER) stress. Here, a genome-wide association study (GWAS) reveals that the transcription factor OsbZIP60 is a vital regulator of rice grain chalkiness. Genetic analysis demonstrates that knockout of OsbZIP60 results in extremely high grain chalkiness and aberrant structure of storage substances. Notably, the expression of unfolded protein response (UPR) genes, such as OsbZIP50, OsBiP1, OsBiP2 and OsBiP3, is up-regulated in the endosperm cells of osbzip60, and overexpression of all these UPR genes causes various degrees of chalkiness. Furthermore, OsbZIP60 is found to activate the expression of key genes related to grain chalkiness, such as GPA3, FSE1, FLO7, Chalk5, OsNF-YB1, and OsPK2, whose expression is significantly suppressed in osbzip60 and overexpression lines of OsbZIP50, OsBiP1, OsBiP2, and OsBiP3. Our study provides novel insights into the function of OsbZIP60 and the role of the UPR pathway in the formation of grain chalkiness in rice.

The genetic control of glabrous glume during African rice domestication

Leqin Chang, Min Hu, Jing Ning, Wei He, Jiayu Gao, Marie-Noelle Ndjiondjop, Yongcai Fu, Fengxia Liu, Hongying Sun, Ping Gu, Chuanqing Sun, Zuofeng Zhu

2022, 49(5): 427-436. doi: 10.1016/j.jgg.2022.02.009

Abstract (480) PDF (32)

Abstract:
African cultivated rice, Oryza glaberrima, is characterized by its glabrous glumes. During domestication, the pubescent glumes of its wild ancestor, Oryza barthii, lost their trichomes, and in this study, we show that glabrous glume 5 (GLAG5), a WUSCHEL-like homeobox transcription factor gene on chromosome 5, is required for trichome development. DNA methylation associated with an hAT transposable element inserted in the promoter region of GLAG5 is found to reduce its expression, leading to the formation of glabrous glumes and leaves in African cultivated rice. Among 82 African cultivated rice varieties investigated in this study, 59 (approximately 71%) lines exhibit glabrous glumes and harbor the hAT transposon; however, the other 23 varieties (approximately 29%), which exhibit pubescent glumes, lack the hAT transposon, indicating that glag5 had undergone strong artificial selection. The π_w/π_c ratios also show the hAT transposon insertions influence the genetic diversity of an approximately 150-kb interval encompassing the GLAG5 locus. The identification of the GLAG5 gene provides new insights into the domestication of cultivated rice in Africa. We speculate that the selection of varieties with mutations in their promoter regions is an important aspect of crop domestication.

Hd1, Ghd7, and DTH8 synergistically determine the rice heading date and yield-related agronomic traits

Kangli Sun, Minghui Huang, Wubei Zong, Dongdong Xiao, Chen Lei, Yanqiu Luo, Yingang Song, Shengting Li, Yu Hao, Wanni Luo, Bingqun Xu, Xiaotong Guo, Guangliang Wei, Letian Chen, Yao-Guang Liu, Jingxin Guo

2022, 49(5): 437-447. doi: 10.1016/j.jgg.2022.02.018

Abstract (364) PDF (40)

Abstract:
Heading date determines the seasonal and regional adaptation of rice (Oryza sativa L.) varieties and is mainly controlled by photoperiod sensitivity (PS). The core heading date genes Hd1, Ghd7, DTH8, and PRR37 act synergistically in regulating the PS. In this study, we systematically analyze the heading date, PS, and agronomic traits of eight homozygous lines with various combinations of Hd1, Ghd7, and DTH8 alleles in the prr37 background under long-day (LD) and short-day (SD) conditions, respectively. We find that Hd1 alone promotes heading, regardless of the day length. However, under LDs, Hd1 suppresses flowering, in coordination with functional Ghd7 or with Ghd7 and DTH8. These loci cooperate to negatively regulate the Ehd1-Hd3a/RFT1 pathway and delay heading. Under SDs, Hd1 competes with various heading suppressors to promote heading. Therefore, the dual function of Hd1 is vital for PS. The lines carrying Hd1 alone show reduced plant height with fewer primary and secondary branches in panicles. Lines carrying Ghd7 and DTH8 (with hd1) show delayed heading and improve agronomic traits. Overall, our results reveal the regulation of rice PS flowering by the core heading date genes and their effects on agronomic traits, providing valuable information for the selection of rice varieties for adaptation to different light and temperature conditions.

Fixation of hybrid sterility genes and favorable alleles of key yield-related genes with dominance contribute to the high yield of the Yongyou series of intersubspecific hybrid rice

Pengfei Wang, Feixiang Qi, Honglin Yao, Xingbing Xu, Wenjun Li, Jianghu Meng, Qinglu Zhang, Weibo Xie, Yongzhong Xing

2022, 49(5): 448-457. doi: 10.1016/j.jgg.2022.02.027

Abstract (200) PDF (27)

Abstract:
In rice, the Yongyou series of Xian-Geng intersubspecific hybrids have excellent production performance, as shown by their extremely high yield. However, the mechanisms underlying the success of these rice hybrids are unclear. In this study, three F₂ populations are generated from three Yongyou hybrids to determine the genetic basis of the extremely high yield of intersubspecific hybrids. Genome constitution analysis reveals that the female and male parental lines belong to the Geng and Xian subspecies, respectively, although introgression of 20% of the Xian ancestry and 14% of the Geng ancestry are observed. Twenty-five percent of the hybrid genomes carries homozygous Xian or Geng fragments, which harbors hybrid sterility genes such as Sd, Sc, f5, and qS12 and favorable alleles of key yield-related genes, including NAL1, Ghd7, and Ghd8. None of the parents carries the S5+ killer of the S5 killer-protector system. Compatible allele combinations of hybrid sterility genes ensure the fertility of these intersubspecific hybrids and overcome the bottleneck in applying intersubspecific hybrids. Additive effects of favorable alleles of yield-related genes fixed in both parents enhances midparent values. Many QTLs for yield and its key component spikelets per panicle shows dominance and the net positive dominant effects lead to heterosis. These factors result in an extremely high yield of the hybrids. These findings will aid in the development of new intersubspecific rice hybrids with diverse genetic backgrounds.

Polyamine oxidase 3 is involved in salt tolerance at the germination stage in rice

Guangyu Liu, Wanxia Jiang, Lei Tian, Yongcai Fu, Lubin Tan, Zuofeng Zhu, Chuanqing Sun, Fengxia Liu

2022, 49(5): 458-468. doi: 10.1016/j.jgg.2022.01.007

Abstract (354) PDF (32)

Abstract:
Soil salinity inhibits seed germination and reduces seedling survival rate, resulting in significant yield reductions in crops. Here, we report the identification of a polyamine oxidase, OsPAO3, conferring salt tolerance at the germination stage in rice (Oryza sativa L.), through map-based cloning approach. OsPAO3 is up-regulated under salt stress at the germination stage and highly expressed in various organs. Overexpression of OsPAO3 increases activity of polyamine oxidases, enhancing the polyamine content in seed coleoptiles. Increased polyamine may lead to the enhance of the activity of ROS-scavenging enzymes to eliminate over-accumulated H₂O₂ and to reduce Na⁺ content in seed coleoptiles to maintain ion homeostasis and weaken Na⁺ damage. These changes resulted in stronger salt tolerance at the germination stage in rice. Our findings not only provide a unique gene for breeding new salt-tolerant rice cultivars but also help to elucidate the mechanism of salt tolerance in rice.

Regulation of nitrogen starvation responses by the alarmone (p)ppGpp in rice

Hanwen Li, Jinqiang Nian, Shuang Fang, Meng Guo, Xiahe Huang, Fengxia Zhang, Qing Wang, Jian Zhang, Jiaoteng Bai, Guojun Dong, Peiyong Xin, Xianzhi Xie, Fan Chen, Guodong Wang, Yingchun Wang, Qian Qian, Jianru Zuo, Jinfang Chu, Xiaohui Ma

2022, 49(5): 469-480. doi: 10.1016/j.jgg.2022.02.006

Abstract (429) PDF (53)

Abstract:
Nitrogen is an essential macronutrient for all living organisms and is critical for crop productivity and quality. In higher plants, inorganic nitrogen is absorbed through roots and then assimilated into amino acids by the highly conserved glutamine synthetase/glutamine:2-oxoglutarate aminotransferase (GS/GOGAT) cycle. How nitrogen metabolism and nitrogen starvation responses of plants are regulated remains largely unknown. Previous studies revealed that mutations in the rice ABNORMAL CYTOKININ RESPONSE1 (ABC1) gene encoding Fd-GOGAT cause a typical nitrogen deficiency syndrome. Here, we show that ARE2 (for ABC1 REPRESSOR2) is a key regulator of nitrogen starvation responses in rice. The are2 mutations partially rescue the nitrogen-deficient phenotype of abc1 and the are2 mutants show enhanced tolerance to nitrogen deficiency, suggesting that ARE2 genetically interacts with ABC1/Fd-GOGAT. ARE2 encodes a chloroplast-localized RelA/SpoT homolog protein that catalyzes the hydrolysis of guanosine pentaphosphate or tetraphosphate (p)ppGpp, an alarmone regulating the stringent response in bacteria under nutritional stress conditions. The are2 mutants accumulate excessive amounts of (p)ppGpp, which correlate with lower levels of photosynthetic proteins and higher amino acid levels. Collectively, these observations suggest that the alarmone (p)ppGpp mediates nitrogen stress responses and may constitute a highly conserved mechanism from bacteria to plants.

OsLTP47 may function in a lipid transfer relay essential for pollen wall development in rice

Libin Chen, Chonghui Ji, Degui Zhou, Xin Gou, Jianian Tang, Yongjie Jiang, Jingluan Han, Yao-Guang Liu, Letian Chen, Yongyao Xie

2022, 49(5): 481-491. doi: 10.1016/j.jgg.2022.03.003

Abstract (310) PDF (36)

Abstract:
In plants, lipid transfer proteins (LTPs) transport pollen wall constituents from the tapetum to the exine, a process essential for pollen wall development. However, the functional cooperation of different LTPs in pollen wall development is not well understood. In this study, we have identified and characterized a grass-specific LTP gene, OsLTP47, an important regulator of pollen wall formation in rice (Oryza sativa). OsLTP47 encodes a membrane-localized LTP and in vitro lipid-binding assays confirms that OsLTP47 has lipid-binding activity. Dysfunction of OsLTP47 causes disordered lipid metabolism and defective pollen walls, leading to male sterility. Yeast two-hybrid and pull-down assays reveal that OsLTP47 physically interacts with another LTP, OsC6. These findings suggest that the plasma membrane-localized OsLTP47 may function as a mediator in a lipid transfer relay through association with cytosolic and/or locular OsC6 for pollen wall development and that various LTPs may function in a coordinated manner to transport lipid molecules during pollen wall development.

Genome-wide selection and introgression of Chinese rice varieties during breeding

Jinyue Ge, Junrui Wang, Hongbo Pang, Fei Li, Danjing Lou, Weiya Fan, Ziran Liu, Jiaqi Li, Danting Li, Baoxuan Nong, Zongqiong Zhang, Yanyan Wang, Jingfen Huang, Meng Xing, Yamin Nie, Xiaorong Xiao, Fan Zhang, Wensheng Wang, Jianlong Xu, Sung Ryul Kim, Ajay Kohli, Guoyou Ye, Weihua Qiao, Qingwen Yang, Xiaoming Zheng

2022, 49(5): 492-501. doi: 10.1016/j.jgg.2022.02.025

Abstract (228) PDF (44)

Abstract:
China is the largest rice-producing country, but the genomic landscape of rice diversity has not yet been clarified. In this study, we re-sequence 1070 rice varieties collected from China (400) and other regions in Asia (670). Among the six major rice groups (aus, indica-I, indica-II, aromatic, temperate japonica, and tropical japonica), almost all Chinese varieties belong to the indica-II or temperate japonica group. Most Chinese indica varieties belong to indica-II, which consists of two subgroups developed during different phases of rice breeding. The genomic segments underlying the differences between these subgroups span 36.32 Mb. The Chinese japonica rice varieties fall into the temperate japonica group, consisting of two subgroups based on their geographical distribution. The genomic segments underlying the differences between these subgroups span 27.69 Mb. These differentiated segments in the Chinese indica varieties span 45 genes with nonsynonymous mutations that are closely related to variations in plant height and grain width. Fifty-four genes with nonsynonymous mutations are associated with the differences in heading date between the two Chinese japonica subgroups. These findings provide new insights into rice diversity in China that will facilitate the molecular breeding.

Nuclear encoded elongation factor EF-Tu is required for chloroplast development in rice grown under low-temperature conditions

Liang Cai, Zongkai Liu, Long Cai, Xiaofeng Yan, Yuan Hu, Benyuan Hao, Zhuang Xu, Yunlu Tian, Xi Liu, Linglong Liu, Ling Jiang, Shirong Zhou, Jianmin Wan

2022, 49(5): 502-505. doi: 10.1016/j.jgg.2021.12.001

Abstract (401) PDF (61)

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Modulating the C-terminus of DEP1 synergistically enhances grain quality and yield in rice

Haixiang Huang, Yafeng Ye, Wenzhen Song, Qi Li, Ruixi Han, Chenchen Wu, Shuoxun Wang, Jianping Yu, Xueying Liu, Xiangdong Fu, Qian Liu, Kun Wu

2022, 49(5): 506-509. doi: 10.1016/j.jgg.2022.01.009

Abstract (654) PDF (126)

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Alanine aminotransferase (OsAlaAT1) modulates nitrogen utilization, grain yield, and quality in rice

Liangbing Fang, Liuyang Ma, Shaolu Zhao, Ruijie Cao, Guiai Jiao, Peisong Hu, Xiangjin Wei

2022, 49(5): 510-513. doi: 10.1016/j.jgg.2022.02.028

Abstract (280) PDF (53)

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SMOC: a smart model for open chromatin region prediction in rice genomes

Weijun Guo, Hanqing Liu, Yifan Wang, Pingxian Zhang, Dongwei Li, Tuoyu Liu, Qian Zhang, Liwen Yang, Li Pu, Jian Tian, Xiaofeng Gu

2022, 49(5): 514-517. doi: 10.1016/j.jgg.2022.02.012

Abstract (358) PDF (24)

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2022 Vol. 49, No. 5