Natural variation at qHd1 affects heading date acceleration at high temperatures with pleiotropism for yield traits in rice

Abstract

BackgroundRice is highly sensitive to temperature fluctuations. Recently, the frequent occurrence of high temperature stress has heavily influenced rice production. Proper heading date in specific environmental conditions could ensure high grain yield. Rice heading greatly depends on the accurate measurement of environmental changes, particularly in day length and temperature. In contrary to the detailed understanding of the photoperiod pathway, little has been known about how temperature regulates the genetic control of rice heading.ResultsNear isogenic lines that were segregated for qHd1, were developed from a cross between indica rice varieties Zhenshan 97 (ZS97) and Milyang 46 (MY46). Using a five sowing-date experiment in the paddy field, we observed the involvement of qHd1 in temperature responses. With the gradual increase of temperature from Trial I to V, heading date of MY46 homozygotes continued to decrease for about 5 d per trial from 76 to 58 d, while that of ZS97 homozygotes was promoted at the same rate from Trial I to III and then stabilized at 69 d. This thermal response was confirmed in a temperature-gradient experiment conducted in the phytotron. It is also found that tolerance of the ZS97 allele to heading acceleration at high temperature was associated with higher grain weight that resulted in higher grain yield. Then, by qRT-PCR and RNA-seq, we found the pathway OsMADS51-Ehd1-RFT1/Hd3a underlying the qHd1-mediated floral response to temperature. By sequence comparison, OsMADS51 for qHd1 displayed a 9.5-kb insertion in the 1st intron of the ZS97 allele compared to the MY46 allele. Furthermore, this large insertion is commonly found in major early-season indica rice varieties, but not in the middle- and late-season ones, which corresponds to the requirement for high-temperature tolerance during the heading and grain-filling stages of early-season rice.ConclusionsBeneficial alleles at qHd1 confer tolerance to high temperatures at the heading and grain-filling stages, playing a significant role in the eco-geographical adaptation of early-season indica rice during modern breeding. These results, together with the underlying OsMADS51-Ehd1-RFT1/Hd3a floral pathway, provide valuable information for better understanding the molecular mechanism of temperature responsive regulation of heading date and yield traits in rice.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1330-5) contains supplementary material, which is available to authorized users.

Loss-of-Function Alleles of Heading date 1 (Hd1) Are Associated With Adaptation of Temperate Japonica Rice Plants to the Tropical Region

“…Temperature is also considered as a major environmental factor in plant flowering although the clear genetic factors have not been demonstrated yet in rice. Recently, the day-length independent flowering QTL, qHd1 encoding OsMADS51 showed reduced heading date in response to increased temperature (Chen et al, 2018). A large insertion (∼9.5 kb) at the first intron of OsMADS51 significantly reduced gene expression and caused tolerance to high temperature-induced flowering.…”

“…Another upstream gene of Ehd1, OsMADS51 , is a flowering activator in SD with major effect and in LD with minor effect (Kim et al, 2007). Recent study by Chen et al (2018) identified that OsMADS51 is also involved in high temperature-induced flowering of rice. Oryza sativa Pseudo-Response Regulator 37 ( OsPRR37 )/ Hd2 also known as Ghd7.1 (Liu et al, 2013) functions as a flowering suppressor in both SD and LD conditions independently of Hd1 and Ehd1 pathways (Koo et al, 2013).…”

Peer Review #1 of "Dissection of three quantitative trait loci for grain size on the long arm of chromosome 10 in rice (Oryza sativa L.) (v0.1)"

“…They inferred that the difference was caused by the temperature difference from flowering to ripening between the two sub-populations, which was higher for the late-maturing sub-population. Similarly, a stronger effect of OsMADS56/qHd1 on grain weight was found to be associated with a higher air temperature (Chen et al, 2018). The average air temperature from flowering to ripening was 23.5C for G10-3 and G10-4, and 27.2C for G11-3 and G11-4.…”

Importance of the Interaction between Heading Date Genes Hd1 and Ghd7 for Controlling Yield Traits in Rice

“…Flowering time is closely related to the grain yield for crop, owing to its key role in maintaining an appropriate balance between full use of resources and avoidance of environmental stresses. Many heading date (HD) genes were reported to affect yield traits, and their natural variations have been used in rice breeding, such as Ghd7 [10], DTH8 / Ghd8 [11,12], Hd1 [13,14], OsPRR37 / Ghd7.1 / DTH7 / Hd2 [15,16,17], RFT1 [18] and OsMADS51 [19,20]. Abiotic stresses during flowering, such as high temperature, low temperature, and drought, can pose a serious threat to spikelet fertility and consequently induce yield loss.…”

“…The relationship between HD gene and abiotic stress has been given attention in recent years. The Ehd1 - Hd3a / RFT1 pathway responses stress signals mediated by Ghd7 [21], OsABF [22] or OsMADS51 [20]. They integrate low temperature, high temperature, and drought signals, respectively, into HD pathway, which induce or repress floral transition to avoid flowering in the stress environments.…”