Artificial selection for a green revolution gene during japonica rice domestication - PubMed (original) (raw)

. 2011 Jul 5;108(27):11034-9.

doi: 10.1073/pnas.1019490108. Epub 2011 Jun 6.

Masanori Yamasaki, Shohei Takuno, Kotaro Miura, Satoshi Katagiri, Tomoko Ito, Kazuyuki Doi, Jianzhong Wu, Kaworu Ebana, Takashi Matsumoto, Hideki Innan, Hidemi Kitano, Motoyuki Ashikari, Makoto Matsuoka

Affiliations

Artificial selection for a green revolution gene during japonica rice domestication

Kenji Asano et al. Proc Natl Acad Sci U S A. 2011.

Abstract

The semidwarf phenotype has been extensively selected during modern crop breeding as an agronomically important trait. Introduction of the semidwarf gene, semi-dwarf1 (sd1), which encodes a gibberellin biosynthesis enzyme, made significant contributions to the "green revolution" in rice (Oryza sativa L.). Here we report that SD1 was involved not only in modern breeding including the green revolution, but also in early steps of rice domestication. We identified two SNPs in O. sativa subspecies (ssp.) japonica SD1 as functional nucleotide polymorphisms (FNPs) responsible for shorter culm length and low gibberellin biosynthetic activity. Genetic diversity analysis among O. sativa ssp. japonica and indica, along with their wild ancestor O. rufipogon Griff, revealed that these FNPs clearly differentiate the japonica landrace and O. rufipogon. We also found a dramatic reduction in nucleotide diversity around SD1 only in the japonica landrace, not in the indica landrace or O. rufipogon. These findings indicate that SD1 has been subjected to artificial selection in rice evolution and that the FNPs participated in japonica domestication, suggesting that ancient humans already used the green revolution gene.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

QTL analysis for CL and isolation of qCL1a. (A and B) Gross morphology (A) and CL (B) of Nipponbare and Kasalath at the mature stage. (Scale bar in A: 20 cm.) Asterisks in B indicate a significant difference (P < 0.001) according to the t test. Error bars represent the SD from the mean (n = 6). (C) QTL analysis for CL in a BIL population. The circles indicate the positions of QTLs, and the circle sizes indicate the relative contribution of each QTL. The red and blue circles indicate QTLs that Nipponbare and Kasalath alleles contribute to the elongation of CL, respectively. qCL1 is marked on chromosome 1. (D) High-resolution mapping of qCL1. (Left) Graphical genotypes of four selected recombinant homozygous lines. The horizontal lines represent chromosome 1, and a physical map is shown for the qCL1 region of chromosome 1. The vertical bars represent the molecular markers. The white and gray bars indicate homozygous alleles of Nipponbare and Kasalath, respectively. (Right) CL for each recombinant homozygous line. Letters (a–d) denote statistically significant differences (P < 0.05) according to Tukey's test. Error bars indicate the SD from the mean (n = 5). (E) Comparison of SD1 amino acid sequences between Nipponbare and Kasalath. The yellow squares and horizontal lines denote the exons and introns of SD1, respectively. The amino acid sequences of GA20ox proteins from Nipponbare, Kasalath, O. rufipogon, maize, barley, wheat, Arabidopsis, pea, tobacco, and tomato were aligned using ClustalW, followed by manual alignment. The red triangles indicate amino acid substitutions between Nipponbare and Kasalath.

Fig. 2.

Fig. 2.

Comparison of the SD1 alleles from Nipponbare and Kasalath. (A) Phenotype of transgenic plants containing the additional SD1 allele: from left to right, transgenic plants containing empty vector (VEC), the Nipponbare allele (N-SD1), and the Kasalath allele (K-SD1). The white arrowheads indicate the position of the panicle node. (Scale bar in A: 20 cm.) (B) CL in transgenic plants containing additional SD1. The letters a and b denote statistically significant differences (P < 0.05) according to Tukey's test. Error bars represent the SD from the mean of the longest culms (n = 15). (C) GA biosynthetic activity of SD1. N.D., not detected. The letters a–c denote statistically significant differences (P < 0.05) according to Tukey's test. Error bars represent the SD from the mean (n = 3).

Fig. 3.

Fig. 3.

Genetic diversity analysis around the SD1 region. (A) Values of π for the silent site of japonica (red circle), indica (blue square), and O. rufipogon (green triangle) across the SD1 genomic region of chromosome 1. (B) Nucleotide variation in japonica or indica relative to O. rufipogon. The blue and red lines indicate the ratios of all site nucleotide diversities in indica and japonica relative to O. rufipogon, respectively. In both A and B, ∼180- to 880-bp portions of 18 flanking genes were sequenced, along with the entire SD1 gene. The approximate genomic locations of the genes are indicated by solid bars, with the following gene identities: 1, hypothetical protein; 2, hypothetical protein; 3, leucine-rich repeat, cysteine-containing containing protein; 4, protein of unknown function, DUF803 family protein; 5, hypothetical protein; 6, SD1; 7, Armadillo-like helical domain containing protein; 8, conserved hypothetical protein; 9, conserved hypothetical protein; 10, similar to AGAMOUS homolog; 11, similar to EMB1879 (EMBRYO DEFECTIVE 1879); 12, hypothetical protein; 13, similar to NAC-domain containing protein 18 (ANAC018) (NO APICAL MERISTEM protein; AtNAM); 14, RIO-like kinase domain-containing protein; 15, similar to LOB domain protein 6 (ASYMMETRIC LEAVES2); 16, hypothetical conserved gene; 17, hypothetical protein; 18, hypothetical conserved gene, and 19, metallophosphoesterase domain-containing protein.

Fig. 4.

Fig. 4.

Phylogenetic trees based on genome-wide transposon insertion patterns (A) and the SD1 genomic sequence (B). Landraces and accessions are indicated by red for japonica, blue for indica, and green for O. rufipogon. Bootstrap values (%) were obtained by 1,000 bootstrap replicates.

Fig. 5.

Fig. 5.

Model of the domestication process in rice. The blue and red circles indicate two genetically distinct groups, indica and japonica, and their corresponding ancestor, O. rufipogon. “GR” enclosed by a blue rectangle or ellipse indicates a GR-type SD1 allele. “EQ” enclosed by red ellipse indicate an EQ-type SD1 allele. Rectangles and ellipses indicate indica and _japonica_-like alleles in relation to sequences outside of the FNPs of SD1, respectively. Genes indicated by blue and red letters are genes introgressed from japonica into indica and genes isolated into the japonica population, respectively.

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