Os08g0105000

Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice

Annotated Information

Function

A number of genes individually controlling number of grains per plant, heading date and plant height have been cloned recently using map-based cloning approaches. Compared with the genes reported previously, Ghd7 is notable in that it has large pleiotropic effects on an array of traits, including grain number,heading date and plant height. Such pleiotropic effects may provide an explanation for QTL hot spots that were observed in many studies. CCT-domain proteins have been reported to have crucial roles in regulating processes such as photoperiodic flowering, vernalization31, circadian rhythms and light signaling. The results of the present study indicate that GHD7 has a key role in photoperiod flowering by regulating the putative Ehd1-Hd3a pathway. Strong expression of Ghd7 in the vascular tissues of leaves is consistent with the role of CO-like genes in flowering regulation. However, we also observed expression of Ghd7 in organs that may not be directly related to photoperiod-controlled flowering, such as roots that do not seem to have a role in flowering, leaves and meristems in the early seedling stage that are much too early for flower induction, and the stems and panicles that already passed the stage of phase transition. Expression in these tissues corresponded well with increases in the various organs leading to an overall increase in plant size, suggesting the possibility that this gene may have a general role in promoting growth, cell proliferation and differentiation, in addition to photoperiod flowering. Ghd7 controls heading date through its enhanced expression under long-day conditions to repress the expression of Hd3a, likely through Ehd1, thus delaying flowering. Of note, the cereal VRN2 gene, although referred to as a vernalization gene, actually has a day-length control and is only expressed under long-day conditions, when it acts as a repressor of flowering. VRN2 was classified in the same CCT subfamily as Ghd7. This suggests that tropical short-day plants that do not use vernalization as a flowering cue, and temperate long-day plants that do use vernalization, actually use related genes to repress flowering in long-day conditions. Such similarity in flowering control provides important clues as to how the temperate cereals might have evolved. Moreover, these genes also act as major sources of adaptive variation, and hence are keys to understanding the spread and success of cereals. Sequence analysis of allelic variants at theGhd7 locus indicated that this locus has contributed greatly to both productivity and adaptability of cultivated rice on a global scale. Asian cultivated rice originated in tropical and subtropical regions of Asia. The functional alleles with strong effects (for example,Ghd7-1 andGhd7-3) allow rice plants to fully exploit light and temperature by delaying flowering under long-day conditions in areas with long growing seasons, thus producing large panicles and increasing yield. The mutations giving rise to the Ghd7-0 and Ghd7-2 alleles, with no or reduced effect of delaying heading under long-day conditions, have had crucial roles by enabling rice to be cultivated under conditions with short growth duration and/or temperate regions. Additionally, the substantial dominant effect observed in the heterozygote between NIL(zs7) and NIL(mh7) indicated that theGhd7 locus has also contributed significantly to the highlevel of heterosis of Shanyou 63 (refs. 19,40), a widely cultivated hybrid in China in the last more than 20 years. Yield has been generally regarded as a complex trait that is controlled by multiple genes of small effects. The major effects demonstrated by the NILs and transgenic plants and the cloning of this QTL have fundamental implications for yield improvement,suggesting that yield, like other traits, can also be improved by individually manipulating the component traits using both molecular marker–assisted selection and transformation. Ghd7 has pleiotropic effects on three agronomic traits (PH, HD, and spikelets per panicle [SPP]). Ghd7 delays HD, increases PH and panicle size, and results in enhanced gene expression of Ehd1 and Hd3a under long-day conditions. Expression pattern analysis suggested that Ghd7 may function upstream of Ehd1 and Hd3a in the rice flowering pathway. Association analysis of 19 rice cultivars identified five allelic variants of Ghd7. The Ghd7 alleles with strong genetic effects were shown to increase grain yield by adapting to the long growing season of tropical regions and the Ghd7 alleles with no or reduced effect found in temperate regions shortened the rice life cycle to ensure seed setting

Expression

Expression pattern of Ghd7

We investigated the diurnal expression pattern ofGhd7 by quantifying the relative abundance of the mRNA in young leaves of NIL(mh7) using quantitative RT-PCR. The expression of Ghd7 was much higher under long-day conditions than short-day conditions, and the Ghd7 transcript was much more abundant during the light period than in dark period, especially under long-day conditions.We carried out RNA in situ hybridization and Ghd7 promoter–driven GFP transformation to examine sites of Ghd7 expression. The RNA in situ hybridization signals indicated that the gene is expressed in young tissues, such as the apical meristem, developing leaves and the leaf sheaths of the young seedling, the meristem of the root, the epidermal layer of developing stems and the branch-primordia of developing panicles. The GFP signal was strong in the young stem and in vascular tissues in the blades of fully expended leaves, but weak in the root and vascular tissues of the leaf sheath.

Evolution

Comparison of the predicted protein sequences identified five alleles that showed a clear geographic distribution. Ghd7-1 was found in rice varieties from the tropics, subtropics and areas with hot summers and long growing seasons, including the most popular high-yield cultivars and parents of elite hybrids in China and Southeast Asia. The wild rice accession also had this allele, indicating that Ghd7-1 is probably the original wild-type allele. Ghd7-2, differing from Ghd7-1 by four amino acids, was found in varieties of temperate japonica from Japan and northern China. This allele seemed to have a smaller phenotypic effect than Ghd7-1. Ghd7-3 occurring in Teqing is distinct from all the other alleles in that it differs by three amino acids from both Ghd7-1 and Ghd7-2, with one variant amino acid found only in this variety. The phenotypic effect ofGhd7-3 seems to be the same magnitude as that of Ghd7-1 (Table 1 and Supplementary Table 4). The remaining two alleles (Ghd7-0 and Ghd7-0a) were nonfunctional. Ghd7-0, with the Ghd7 locus completely deleted, was found in two varieties grown as early rice in a system with two-rice crops in central and southern China, in which the growth duration for early rice is short. Ghd7-0a, resulting from a premature termination in the predicted coding region, was found in two varieties from the Heilongjiang Province of northeastern China, which has cool summers and a short growing season.

Labs working on this gene

National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.

References

[1]Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Gent 40:761-767