Cytological mechanism of pollen abortion resulting from allelic interaction of F1 pollen sterility locus in rice (Oryza sativa L.)

Zhang, Zhisheng; Lu, Yue; Liu, Xiangdong; Feng, Jiancan; Zhang, Guiquan

doi:10.1007/s10709-005-4848-z

Cited by 34 publications

(39 citation statements)

References 12 publications

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“…In plants, after the first description of a PK in a hybrid between two Solanum species (Cameron and Moav 1957), gamete killers (most often PKs) have been reported, especially in hybrids between cultivated plants and their wild relatives, where they often constitute obstacles to the breeding of desirable traits (Maan 1975;Sano 1990). In rice in particular, a number of gamete killers have been described in crosses between cultivated rice (O. sativa) and its wild relatives (Sano 1990;Hu et al 2006;Garavito et al 2010), or between O. sativa subspecies (Oka 1974;Zhang et al 2006). The genes underlying two of the latter have been identified (Chen et al 2008;Long et al 2008;Yang et al 2012).…”

Section: Discussionmentioning

confidence: 99%

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

et al. 2016

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Species differentiation and the underlying genetics of reproductive isolation are central topics in evolutionary biology. Hybrid sterility is one kind of reproductive barrier that can lead to differentiation between species. Here, we analyze the complex genetic basis of the intraspecific hybrid male sterility that occurs in the offspring of two distant natural strains of Arabidopsis thaliana, Shahdara and Mr-0, with Shahdara as the female parent. Using both classical and quantitative genetic approaches as well as cytological observation of pollen viability, we demonstrate that this particular hybrid sterility results from two causes of pollen mortality. First, the Shahdara cytoplasm induces gametophytic cytoplasmic male sterility (CMS) controlled by several nuclear loci. Second, several segregation distorters leading to allele-specific pollen abortion (pollen killers) operate in hybrids with either cytoplasm. The complete sterility of the hybrid with the Shahdara cytoplasm results from the genetic linkage of the two causes of pollen mortality, i.e., CMS nuclear determinants and pollen killers. Furthermore, natural variation at these loci in A. thaliana is associated with different malesterility phenotypes in intraspecific hybrids. Our results suggest that the genomic conflicts that underlie segregation distorters and CMS can concurrently lead to reproductive barriers between distant strains within a species. This study provides a new framework for identifying molecular mechanisms and the evolutionary history of loci that contribute to reproductive isolation, and possibly to speciation. It also suggests that two types of genomic conflicts, CMS and segregation distorters, may coevolve in natural populations.

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Section: Discussionmentioning

confidence: 99%

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

et al. 2016

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“…5B). Because the male developmental defect appears at the early uni-nucleate microspore stage (20), the protein transport may occur at the tetrad stage, through cytoplasmic channels existing between tetrad cells (27). However, SaM Ϫ should be unable to move to the microspores carrying SaM ϩ to cause sterility, probably because of the loss of a necessary domain in the truncated region.…”

Section: Discussionmentioning

confidence: 99%

“…1 A-C). The male developmental defect caused by heterozygous Sa appeared in microspores of the early uni-nucleate stage (20), but female fertility was unaffected (15,16). Of 666 analyzed F 2 plants, only three (0.45%) were of Sa j /Sa j ; the others were either Sa i /Sa j or Sa i /Sa i , with distribution being equal ( Fig.…”

Section: Genetic Effect Of Sa On Hybrid Male Sterilitymentioning

confidence: 95%

Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes

Long

Zhao

Niu

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

232

257

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Sterility is common in hybrids between divergent populations, such as the indica and japonica subspecies of Asian cultivated rice (Oryza sativa). Although multiple loci for plant hybrid sterility have been identified, it remains unknown how alleles of the loci interact at the molecular level. Here we show that a locus for indicajaponica hybrid male sterility, Sa, comprises two adjacent genes, SaM and SaF, encoding a small ubiquitin-like modifier E3 ligase-like protein and an F-box protein, respectively. 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. We propose a two-gene/threecomponent interaction model for this hybrid male sterility system. The findings have implications for overcoming male sterility in inter-subspecific hybrid rice breeding.allelic interaction ͉ gamete selection ͉ hybrid sterility ͉ reproductive barrier ͉ two-gene/three-component model

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“…Interestingly, the Skn-1_motif, which is required for endosperm development (Lescot et al, 2002), was the main type of regulatory element present in the promoter regions of these 55 genes (Supplemental Table S7). Partial pollen sterility and embryo sac abortions affect seed setting of intersubspecific rice hybrids and limit the commercial production of hybrids (Zhang and Lu, 1989;Zhang et al, 2006;Ji et al, 2012;Shahid et al, 2013a). Six loci, including Sa, Sb, Sc, Sd, Se, and Sf, have been found to regulate intersubspecific rice hybrid pollen sterility Lu, 1989, 1993;Zhang et al, 1994).…”

Section: Coexpression and Cis-motif Analysis Of Meiosis-related Or Stmentioning

confidence: 99%

“…Each locus interaction (S i S j ) caused partial pollen sterility in intersubspecific hybrids (Zhang and Lu, 1989). Transmission electron microscopy revealed that Sa allelic interactions caused microspore abnormalities at the middle microspore stage and finally, produced empty abortive pollen; Sb allelic interactions resulted in asynchronous development of microspores at the middle microspore stage, producing stainable abortive pollen, and Sc allelic interactions mainly led to the nondissolution of the generative cell wall and finally, produced stainable abortive pollen (Zhang et al, 2006). In this study, we used Taichung65 and its PSIL to generate a diploid hybrid with Sa, Sb, and Sc loci interactions.…”

Section: Coexpression and Cis-motif Analysis Of Meiosis-related Or Stmentioning

confidence: 99%

Polyploidy enhances F1 pollen sterility loci interactions that increase meiosis abnormalities and pollen sterility in autotetraploid rice

Shahid

Chen

et al. 2015

Plant Physiol.

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Intersubspecific autotetraploid rice (Oryza sativa ssp. indica 3 japonica) hybrids have greater biological and yield potentials than diploid rice. However, the low fertility of intersubspecific autotetraploid hybrids, which is largely caused by high pollen abortion rates, limits their commercial utility. To decipher the cytological and molecular mechanisms underlying allelic interactions in autotetraploid rice, we developed an autotetraploid rice hybrid that was heterozygous (S i S j ) at F 1 pollen sterility loci (Sa, Sb, and Sc) using near-isogenic lines. Cytological studies showed that the autotetraploid had higher percentages (.30%) of abnormal chromosome behavior and aberrant meiocytes (.50%) during meiosis than did the diploid rice hybrid control. Analysis of gene expression profiles revealed 1,888 genes that were differentially expressed between the autotetraploid and diploid hybrid lines at the meiotic stage, among which 889 and 999 were up-and down-regulated, respectively. Of the 999 down-regulated genes, 940 were associated with the combined effect of polyploidy and pollen sterility loci interactions (IPE). Gene Ontology enrichment analysis identified a prominent functional gene class consisting of seven genes related to photosystem I (Gene Ontology 0009522). Moreover, 55 meiosis-related or meiosis stage-specific genes were associated with IPE in autotetraploid rice, including Os02g0497500, which encodes a DNA repair-recombination protein, and Os02g0490000, which encodes a component of the ubiquitin-proteasome pathway. These results suggest that polyploidy enhances epistatic interactions between alleles of pollen sterility loci, thereby altering the expression profiles of important meiosis-related or meiosis stage-specific genes and resulting in high pollen sterility.

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Cytological mechanism of pollen abortion resulting from allelic interaction of F1 pollen sterility locus in rice (Oryza sativa L.)

Cited by 34 publications

References 12 publications

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes

Polyploidy enhances F1 pollen sterility loci interactions that increase meiosis abnormalities and pollen sterility in autotetraploid rice

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