Nonfunctional alleles of long-day suppressor genes independently regulate flowering time

Abstract

Due to the remarkable adaptability to various environments, rice varieties with diverse flowering times have been domesticated or improved from Oryza rufipogon. Detailed knowledge of the genetic factors controlling flowering time will facilitate understanding the adaptation mechanism in cultivated rice and enable breeders to design appropriate genotypes for distinct preferences. In this study, four genes (Hd1, DTH8, Ghd7 and OsPRR37) in a rice long-day suppression pathway were collected and sequenced in 154, 74, 69 and 62 varieties of cultivated rice (Oryza sativa) respectively. Under long-day conditions, varieties with nonfunctional alleles flowered significantly earlier than those with functional alleles. However, the four genes have different genetic effects in the regulation of flowering time: Hd1 and OsPRR37 are major genes that generally regulate rice flowering time for all varieties, while DTH8 and Ghd7 only regulate regional rice varieties. Geographic analysis and network studies suggested that the nonfunctional alleles of these suppression loci with regional adaptability were derived recently and independently. Alleles with regional adaptability should be taken into consideration for genetic improvement. The rich genetic variations in these four genes, which adapt rice to different environments, provide the flexibility needed for breeding rice varieties with diverse flowering times.

Keywords: Domestication; flowering time; long-day suppressor genes; loss-function allele; rice.

Figure 1

Sequence polymorphism analysis of the Hd1, DTH8, Ghd7 and OsPRR37 coding regions in cultivars of rice Wild types, which are the type of first accession in sequence alignment, are represented by dashes and variations that would lead genes to be nonfunctional are in yellow. The length of indels, which is more than 25, is represented by letter. The sequence information for each letter reads as follows. a:GCCAGGCGCCACCAGCGCGTCCCCGTCGCGCCGCTC; b:GACAACAGCAACAGCAACAGCAGCAAC; c:AACAACAACGACAACGACAATAACGACAACAAC; d:AGGTACAATTCGTACTACGACAACAAC; e:AATAACGACAACAGCAACAGCAACAGCAGCAACAACGACAACGACAACGACAA; f:TAACAACAACAGCAACAGCAGCAACAACGGCATGTATTTTGGTGAAGTCGATGAGTACTTTGATCTTGTCAGGTACAATTCGTACTACGACAACAAC; g:AATAACGACAACAGCAACAGCAACAGCAGCAACAACGACAACGACAACGAC; h:AATAACAACAACAGCAACAGCAGCAACAACGGCATGTATTTTGGTGAAGTCGATGAGTACTTTGATCTTGTC; i:ACCTTCACAGATCACAATGCTGAGTGAGCAGCAGCATAGTGGT; j:GTTAGGAAATAAACCTGACCGTGTGTGTTCAGGTCAGTTCGCGTGCGTCGTGTGTGTGTTTGTTGTTGAACGCGTCCGTCGTGTGGAGGTTCGTCCGAGTTTTAGCGCAGGCTAGCTAGCTGCGAGCGTGTGTATCGGGTTCAGTTGGAGAGTGTGGCGTCGTGCGCGGACGCTGGCGGCCGCGTCGTGCGCTGAGTTTGTGCTCATGCATGGCGTGAGCCGGGACGTGCGGATCGTGCGAGCAAAGGCCGGGGAAGGAGTTCGTGCTCCATTTGTGCGTCACCCTGGGCCTATATAAGCACATGTTCATCCCGTTGTTGATCACCGAGTGAAAAAAAAGAAAAGCCGGCATTCGTTGCCAGGGCGTTCGTTGCCATTGTCAAGCTTCACAAACTCTGCTACTCACTCTCGTGTTTGTGTGTGTCTCCGATCTTGGCCATTTCCAACATATAGT.

Figure 2

Variation in flowering time of cultivars Comparison of flowering times between accessions with nonfunctional and functional alleles. The yellow and blue bars represent nonfunctional (NON) and functional (FUN) alleles of Hd1, DTH8, Ghd7 and OsPRR37, respectively. FT is the abbreviation of flowering time. P values were produced by two‐tailed t‐tests and Wilcoxon signed‐rank tests. Flowering time in each accession is mean ± SD (standard deviations).

Figure 3

Distribution map of rice landraces carrying the nonfunctional alleles (A) Hd1. (B) DTH8. (C) Ghd7. (D) OsPRR37. Each circle represents one accession. Each color represents different haplotypes except that alleles with less than three varieties are shown in pink.

Figure 4

Allele network analysis for four loci (A) Hd1. (B) DTH8. (C) Ghd7. (D) OsPRR37. Allele frequencies are proportional to circle size. The proportions of the two rice subspecies (indica and japonica) are represented by gray and black, respectively. Circles with red borders indicate nonfunctional alleles and circles with black borders indicate functional alleles. Lines connect two alleles with the most recent relationships. The number on the lines between the circles indicates the evolutionary distance between the two alleles.