Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development

Hanson, Maureen R.; Bentolila, Stéphane

doi:10.1105/tpc.015966

Cited by 746 publications

(644 citation statements)

References 140 publications

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“…This provides a simple mechanism for effects of restorer segregation (in a CMS background) on floral morphology in our hybrids, and may also contribute to the common observation that male-sterile (female) flowers are smaller in many gynodioecious taxa (Baker, 1948;Delph et al, 1996;Eckhart, 1999). Our results are also consistent with observations in crop CMS hybrids, in which cytoplasmic type has a variety of effects on floral morphology in addition to fertility (Zubko et al, 2003;Hanson and Bentolila, 2004). However, we note that selection for increased allocation to corollas via male fitness in hermaphrodites (for example, Bell, 1985;Ashman and Stanton, 1991;Johnson et al, 1995) could accentuate initial differences due to direct developmental effects.…”

Section: Discussionsupporting

confidence: 81%

“…Gibberellins are important for cell elongation and the tapetum, a layer of cells in the anther surrounding the microspores, is the site of some of the highest expression of gibberellic acid synthesis genes (for example, Kaneko et al, 2003). Tapetal degeneration and pollen abortion, a characteristic of CMS in crop systems (Hanson and Bentolila, 2004) is prevented by pentatricopeptide (PPR) restorers, such as those identified in this Mimulus system (Barr and Fishman, 2010). This provides a simple mechanism for effects of restorer segregation (in a CMS background) on floral morphology in our hybrids, and may also contribute to the common observation that male-sterile (female) flowers are smaller in many gynodioecious taxa (Baker, 1948;Delph et al, 1996;Eckhart, 1999).…”

Section: Discussionmentioning

confidence: 99%

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Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

Barr

Fishman

2011

Heredity

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The mechanisms underlying genetic associations have important consequences for evolutionary outcomes, but distinguishing linkage from pleiotropy is often difficult. Here, we use a fine mapping approach to determine the genetic basis of association between cytonuclear male sterility and other floral traits in Mimulus hybrids. Previous work has shown that male sterility in hybrids between Mimulus guttatus and Mimulus nasutus is due to interactions between a mitochondrial gene from M. guttatus and two tightly linked nuclear restorer alleles on Linkage Group 7, and that male sterility is associated with reduced corolla size. In the present study, we generated a set of nearly isogenic lines segregating for the restorer region and male sterility, but with unique flanking introgressions. Male-sterile flowers had significantly smaller corollas, longer styles and greater stigmatic exsertion than fertile flowers. Because these effects were significant regardless of the genotypic composition of introgressions flanking the restorer region, they suggest that these floral differences are a direct byproduct of the genetic incompatibility causing anther abortion. In addition, we found a non-significant but intriguing trend for male-sterile plants to produce more seeds per flower than fertile siblings after supplemental pollination. Such pleiotropic effects may underlie the corolla dimorphism frequently observed in gynodioecious taxa and may affect selection on cytoplasmic male sterility genes when they initially arise.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

Barr

Fishman

2011

Heredity

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“…As Mg 2+ is a critical cofactor of ATP synthases and other enzymes in the respiration processes, Mg 2+ level should serve as an essential regulatory element of mitochondrial activity. As mitochondrial defects have long been implicated in male sterility, it is not fortuitous that AtMGT5 plays an essential role in pollen development [26][27][28][29]. Although due to technical difficulty the sub-cellular localization of AtMGT9 protein has not been determined, it stands as a possibility that this transporter may also be localized in the mitochondria and regulate Mg 2+ homeostasis in this organelle.…”

Section: Discussionmentioning

confidence: 99%

Magnesium transporter AtMGT9 is essential for pollen development in Arabidopsis

Chen

Liu

et al. 2009

Cell Res

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Magnesium (Mg 2+ ) is abundant in plant cells and plays a critical role in many physiological processes. A 10-member gene family AtMGT (also known as AtMRS2) was identified in Arabidopsis, which belongs to a eukaryote subset of the CorA superfamily, functioning as Mg 2+ transporters. Some family members (AtMGT1 and AtMGT10) function as high-affinity Mg 2+ transporter and could complement bacterial mutant or yeast mutant lacking Mg 2+ transport capability. Here we report an AtMGT family member, AtMGT9, that functions as a low-affinity Mg 2+ transporter, and is essential for pollen development. The functional complementation assay in Salmonella mutant strain MM281 showed that AtMGT9 is capable of mediating Mg 2+ uptake in the sub-millimolar range of Mg 2+ . The AtMGT9 gene was expressed most strongly in mature anthers and was also detectable in vascular tissues of the leaves, and in young roots. Disruption of AtMGT9 gene expression resulted in abortion of half of the mature pollen grains in heterozygous mutant +/mgt9, and no homozygous mutant plant was obtained in the progeny of selfed +/mgt9 plants. Transgenic plants expressing AtMGT9 in these heterozygous plants can recover the pollen phenotype to the wild type. In addition, At-MGT9 RNAi transgenic plants also showed similar abortive pollen phenotype to mutant +/mgt9. Together, our results demonstrate that AtMGT9 functions as a low-affinity Mg 2+ transporter that plays a crucial role in male gametophyte development and male fertility.

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“…Both Rf loci occur within a cluster of tandemly repeated PPR genes, and LG7 contains the highest concentration of restorer-like PPRs in the M. guttatus genome [33]. Thus, the molecular basis of the CMS-Rf system in Mimulus resembles the cryptic CMS seen in diverse crop hybrids [30], and is probably representative of evolutionary processes commonly occurring throughout flowering plants [31,34].…”

Section: Introductionmentioning

confidence: 99%

“…Regardless of their direct role as species barriers, cytonuclear incompatibilities manifest fundamental and theoretically widespread processes of nuclear and organellar coevolution. Cytonuclear hybrid male sterility is extremely common in angiosperms [21], and cross-species patterns of molecular evolution suggest a long-term history of conflict between CMS and the widespread class of nuclear Rf genes ( pentatricopeptide repeat genes, PPRs; [30,31]). Selfish models of CMS-Rf coevolution are widely accepted, but the history of natural selection on Rf or CMS loci has not been demonstrated in any system.…”

Section: Introductionmentioning

confidence: 99%

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

et al. 2016

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Intraspecific coevolution between selfish elements and suppressors may promote interspecific hybrid incompatibility, but evidence of this process is rare. Here, we use genomic data to test alternative models for the evolution of cytonuclear hybrid male sterility in Mimulus. In hybrids between Iron Mountain (IM) Mimulus guttatus Â Mimulus nasutus, two tightly linked M. guttatus alleles (Rf1/Rf2) each restore male fertility by suppressing a local mitochondrial male-sterility gene (IM-CMS). Unlike neutral models for the evolution of hybrid incompatibility loci, selfish evolution predicts that the Rf alleles experienced strong selection in the presence of IM-CMS. Using whole-genome sequences, we compared patterns of population-genetic variation in Rf at IM to a neighbouring population that lacks IM-CMS. Consistent with local selection in the presence of IM-CMS, the Rf region shows elevated F ST , high local linkage disequilibrium and a distinct haplotype structure at IM, but not at Cone Peak (CP), suggesting a recent sweep in the presence of IM-CMS. In both populations, Rf2 exhibited lower polymorphism than other regions, but the low-diversity outliers were different between CP and IM. Our results confirm theoretical predictions of ubiquitous cytonuclear conflict in plants and provide a population-genetic mechanism for the evolution of a common form of hybrid incompatibility.

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Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development

Cited by 746 publications

References 140 publications

Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

Magnesium transporter AtMGT9 is essential for pollen development in Arabidopsis

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

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