Os01g0578500

SaF+/SaF- is an important gene impact the fertility in hybrids between indica and japonica subspecies of Asian cultivated rice(Oryza sativa).

Annotated Information

Function

Sterility is common in hybrids between divergent populations,such as the indica and japonica subspecies of Asian cultivated rice(Oryza sativa).SaF is one gene of the Sa locus,which include two adjacent genes SaF and SaM.SaM encoding a small ubiquitin-like modifier E3 ligase-like protein and an F-box protein. Most indica cultivars contain a haplotype SaM+SaF+,whereas all japonica cultivars have SaM-SaF- that diverged by nucleotide variations in wild rice. Male semi-sterility in this heterozygous complex locus is caused by abortion of pollen carrying SaM-. This allele-specific gamete elimination results from a selective interaction of SaF+ with SaM-, a truncated protein, but not with SaM+ because of the presence of an inhibitory domain, although SaM+ is required for this male sterility. Lack of any one of the three alleles in recombinant plants does not produce male sterility.

SaF Interacts with SaM- but not with SaM+. A bacterial two-hybrid(B2H) interaction assay demonstrated that both SaF+ and SaF- interacted physically with SaM- but not with SaM+.Therefore, the amino acid substitution in SaF- did not affect its physical interaction with SaM- but impaired the biological function of SaF-for male sterility.There is a self-inhibitory domain within the 203–218 region of SaM+ blocks the interaction, probably by affecting the protein’s structure.

Functional analysis of SaM+,SaM-,and SaF+ in rice by transformation indicate that the segregation distortion of the Sa region is a consequence of hybrid male sterility caused by the allele-specific gamete selection.

A Molecular Genetic Model for Rice Hybrid Male Sterility.

The absence of any one of the three alleles, SaM+,SaM-,or SaF+, fails to produce male sterility.In an F1 plant, the linked allelesets (SaM+SaF+, SaM-SaF-) are separated from each other in the haploid microspores. Therefore, the SaF+ and SaM+ proteins may need to be transported from their own microspores to those carrying SaM- for interaction. The SaF+ -SaM- complex may interact further with SaM+ indirectly to trigger a specific sterility process. Because the male developmental defect appears at the early uni-nucleate microspore stage, the protein transport may occur at the tetrad stage, through cytoplasmic channels existing between tetrad cells. However, SaM- should be unable to move to the microspores carrying SaM+ to cause sterility, probably because of the loss of a necessary domain in the truncated region. The selective protein transport and the specific SaF+ -SaM- interaction restrict the sterility process in the SaM--containing microspores, thereby resulting in allele-specific pollen killing. This model also can explain the induction of male sterility in other recombinants and in the transgenic plants.In some of these plants, SaF+(tSaF+) and/or SaM+ (tSaM+) co-exist with SaM- (tSaM-) in microspores, and the transgenes can function by ectopic expression to cause male sterility. Therefore, the molecular effect of the ‘‘allelic interaction’’ of gene sets does not necessarily require genetic allelism (i.e., location at the same position of the chromosomes). In conclusion, SaM- acts as a gametophytic factor in the male sterility system, whereas SaM+ and SaF+ play their roles in any microspores in which they are located. On the other hand, the blocking of the SaF+–SaM- interaction by the self-inhibitory domain in SaM+ may be an important mechanism to prevent triggering the sterility process in SaM+-carrying microspores, thus facilitating its transmission to hybrid progenies and avoiding male sterility in indica cultivars.

Expression

SaF encodes a 476-aa protein with an F-box and a plantspecific F-box protein domain (FBD). F-box proteins mediate protein–protein interactions, but the function of the FBD is unclear. The SaF protein is homologous to a ribosomal RNA apurinic site-specific lyase (RALyase) in wheat (23) with 33% identity in the overall sequences and 64% and 44% identities in the F-box and FBD, respectively. About 20 members of the F-box/FBD subfamily are predicted in rice, and they have up to 75% identity to RALyase and up to 40% identity to SaF.In the coding region of SaF, only one SNP was found between SaF-and SaF+, which results in a Phe-to-Ser substitution in position 287. SaF was expressed in all tissues tested as examined by RT-PCR, albeit at different levels.This analysis showed that only the cDNA of SaF was detectable in the purified pollen of the F1 plants, providing molecular evidence for the selective abortion of SaF-carrying pollen.

Evolution

Divergence of SaM and SaF Arose in Wild Rice Species.

To trace the origins of the variation in SaF and SaM,the SNPs G02-69.8 and G02-74.6 was investigated in 13 wild species and in cultivated rice. The nucleotides "T" and "C" at G02-69.8 were variably present in populations of nine wild species (including the common wild rice, O.rufipogon Griff) and in indica cultivars. For G02-74.6, only the nucleotide "G" was detected in all tested wild species and indica, with the exception of O.rufipogon, which was"G"-only in accessions distributing in South and Southeast Asia but contained both "G" and "T" (54 of 110 accessions carried "T") in the accessions from southern China.

In summary, three haplotypes of the linked orthologs, SaM+SaF+, SaM+SaF-, and SaM-SaF-, were present in the O.rufipogon populations. Most indica cultivars (95 of 106 accessions) contained SaM+SaF+, but 11 accessions carried SaM+SaF-. All the tested 108 japonica cultivars possessed SaM-SaF-. These results indicate that the variation in SaF occurred before the split of most, if not all, of the Oryza species, whereas the mutation in SaM most likely arose in an O. rufipogon population with SaM+SaF- in southern China and generated the haplotype SaM-SaF- .

Labs working on this gene

Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Province, College of Life Sciences, South China Agricultural University, Wushan, Guangzhou 510642, China

References

[1] Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, Xia J, Wang L, Wu H and Liu Y-G* . 2008. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc. Natl. Acad. Sci. USA. 105(48):18871-18876.