[Intellectual contribution]

An SNP caused loss of seed shattering during rice domestication

Takeshi IZAWA¹, Saeko KONISHI², Masahiro YANO³

¹ Plant Genome Research Unit & Photobiology and Photosynthesis Research Unit, NIAS, ² STAFF Institute, ³ QTL Genome Breeding Center, NIAS

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   Rice (Oryza sativa) is a staple food for human beings and it is believed that rice was domesticated around ten thousand years ago. It was long assumed that a single major domestication process occurred which produced a subspecies of rice and that subsequent artificial selection upon existing variation resulted in rice cultivar groups such as indica, tropical japonica, and temperate japonica. Recent genome analysis revealed that this assumption might be wrong because an indica cultivar ‘93-11’ and a japonica cultivar ‘Nipponbare’ became diversified about 0.2^~0.4 million years ago based on phylogenetic analyses of retrotransposon distribution. Therefore, several independent domestication processes may have occurred to make the diversity of these subspecies in rice. However, it is not well understood how the domestication process took place at the molecular level.
   Here, we first performed QTL (quantitative trait locus) analysis for the seed shattering trait, one of the domestication traits, between an indica cultivar (Kasalath) and a japonica cultivar (Nipponbare)(Fig. 1) and detected five QTL loci involved in seed shattering. We next cloned a major gene termed qSH1 (QTL of seed shattering in chromosome 1). qSH1 encodes a Bell-type homeobox transcription factor which is an ortholog of REPLUMLESS (RPL) gene in Arabidopsis thaliana. RPL was reported to be involved in formation of the abscission layer in A. thaliana fruit. Indeed, a nearly isogenic line, NIL (qSH1), containing a Kasalath genome fragment corresponding to the qSH1 region, restored formation of the separation layer at the bottom of rice grains which shattered easily (Fig. 2). These results indicate that qSH1 is required for the abscission layer formation in rice and, thus, revealed that an evolutionarily conserved molecular mechanism is involved in the separation layer formation regardless of the botanical origin of the layers.
    Fine mapping of qSH1 also led us to identify a single nucleotide polymorphism (SNP) which caused the loss of seed shattering. In situ expression analysis of qSH1 mRNA (Fig. 3) and complementation tests using 12 Kasalath genome fragments further demonstrated that this SNP conferred loss of abscission layerspecific transcription of qSH1. These results suggested that ancient humans likely selected this SNP for loss of seed shattering due to the defect in formation of the separation layer.
    We further analyzed haplotypes of the qSH1 gene using several rice core collections. These analyses revealed that the SNP was introduced into rice cultivars after the diversification of temperate japonica. When temperate japonica cultivars of Chinese origin were tested, we found that that the SNP was likely to have occurred as a mutation in ancient China. Since it is believed that rice cultivation was introduced into Japan at least 3000 years ago, the mutation for SNP is likely to have occurred more than 3000 years ago.
    Therefore, we finally concluded that the loss of seed shattering occurred in the early domestication of temperate japonica more than 3000 years ago and then ancient humans in China selected rice plants with this specific SNP to improve yields due to the decrease of seed dispersal (Fig. 4).

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Fig. 1  Seed shattering habits of rice panicles (left) and chromosomal locations of QTLs for seed shattering degree (right)

Fig. 2  Left: Photo of a rice grain White box indicates position of abscission layer formation. Middle and right: Longitudinal sections of positions corresponding to white box The corresponding region of Nipponbare (middle) and the completed abscission layer of NIL (qSH1)(right).

Fig. 3  In situ analysis of qSH1 expression At flower formation stage, qSH1 expression was detected in anther regions in both NIL (qSH1) and Nipponbare (left) and at the provisional abscission layer position only in NIL (qSH1)(right) and not in Nipponbare.

Fig. 4  The origin of the identified SNP

 

 

[Reference]

Konishi S, Izawa T, Lin S-Y, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science, 312: 1392-1396.

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