Extensive Rearrangement of the Arabidopsis Mitochondrial Genome Elicits Cellular Conditions for Thermotolerance

Shedge, Vikas; Davila, Jaime; Arrieta-Montiel, Maria P.; Mohammed, Saleem; Mackenzie, Sally A.

doi:10.1104/pp.109.152827

Cited by 80 publications

(73 citation statements)

References 36 publications

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“…New mitochondrial genes may provide unique sources of genetic variation that have phenotypic consequences. These consequences can benefit natural adaptation and prove useful for crop breeding [10,42,[49][50][51]. In addition, the new CMS genes identified in this study could greatly expand the germplasm for hybrid rice breeding.…”

Section: Discussionmentioning

confidence: 97%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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New gene origination is a major source of genomic innovations that confer phenotypic changes and biological diversity. Generation of new mitochondrial genes in plants may cause cytoplasmic male sterility (CMS), which can promote outcrossing and increase fitness. However, how mitochondrial genes originate and evolve in structure and function remains unclear. The rice Wild Abortive type of CMS is conferred by the mitochondrial gene WA352c (previously named WA352) and has been widely exploited in hybrid rice breeding. Here, we reconstruct the evolutionary trajectory of WA352c by the identification and analyses of 11 mitochondrial genomic recombinant structures related to WA352c in wild and cultivated rice. We deduce that these structures arose through multiple rearrangements among conserved mitochondrial sequences in the mitochondrial genome of the wild rice Oryza rufipogon, coupled with substoichiometric shifting and sequence variation. We identify two expressed but nonfunctional protogenes among these structures, and show that they could evolve into functional CMS genes via sequence variations that could relieve the self-inhibitory potential of the proteins. These sequence changes would endow the proteins the ability to interact with the nucleus-encoded mitochondrial protein COX11, resulting in premature programmed cell death in the anther tapetum and male sterility. Furthermore, we show that the sequences that encode the COX11-interaction domains in these WA352c-related genes have experienced purifying selection during evolution. We propose a model for the formation and evolution of new CMS genes via a "multi-recombination/protogene formation/functionalization" mechanism involving gradual variations in the structure, sequence, copy number, and function.

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Section: Discussionmentioning

confidence: 97%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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“…Epigenomic changes appear to underlie at least some of the environmentally responsive phenotypic plasticity observed in natural systems (Bonduriansky and Day, 2009). In fact, MSH1 transcript levels show environmental responsiveness, with dramatically reduced levels under conditions of stress (Hruz et al, 2008;Shedge et al, 2010;Xu et al, 2011). Moreover, disruption of MSH1 produces an altered redox state of the plastid , implying one means of signaling cellular change.…”

Section: Discussionmentioning

confidence: 99%

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

Santamaria

Virdi

et al. 2012

Plant Physiology

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Multicellular eukaryotes demonstrate nongenetic, heritable phenotypic versatility in their adaptation to environmental changes. This inclusive inheritance is composed of interacting epigenetic, maternal, and environmental factors. Yet-unidentified maternal effects can have a pronounced influence on plant phenotypic adaptation to changing environmental conditions. To explore the control of phenotypy in higher plants, we examined the effect of a single plant nuclear gene on the expression and transmission of phenotypic variability in Arabidopsis (Arabidopsis thaliana). MutS HOMOLOG1 (MSH1) is a plant-specific nuclear gene product that functions in both mitochondria and plastids to maintain genome stability. RNA interference suppression of the gene elicits strikingly similar programmed changes in plant growth pattern in six different plant species, changes subsequently heritable independent of the RNA interference transgene. The altered phenotypes reflect multiple pathways that are known to participate in adaptation, including altered phytohormone effects for dwarfed growth and reduced internode elongation, enhanced branching, reduced stomatal density, altered leaf morphology, delayed flowering, and extended juvenility, with conversion to perennial growth pattern in short days. Some of these effects are partially reversed with the application of gibberellic acid. Genetic hemicomplementation experiments show that this phenotypic plasticity derives from changes in chloroplast state. Our results suggest that suppression of MSH1, which occurs under several forms of abiotic stress, triggers a plastidial response process that involves nongenetic inheritance.

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“…To select these genes, we assembled a compendium of 12 publicly available and microarray-derived transcriptome data sets that encompassed 22 perturbation experiments in which mitochondrial function was impaired by short-term treatments with respiratory inhibitors or by genetic mutation of mitochondrial proteins: oligomycin and rotenone (Clifton et al, 2005); AOX1a-overexpressing and knockout mutants (35S:AOX1a and aox1a) (National Center for Biotechnology Information Gene Expression Omnibus database; Edgar et al, 2002; accession number GSE4113); 35S:PROHIBITIN3 (PHB3), 35S:PHB4; phb3 and phb4 (Van Aken et al, 2007); aox1a ; mutants defective in NADH dehydrogenase (ubiquinone) fragment S subunit 4 and fragment A subunit 1 ; RNA polymerase of the T3/T7 type dual-targeted to mitochondria and plastids mutants (Kühn et al, 2009); MutS Homolog1 and RECA homolog3 double mutant (Shedge et al, 2010); mitochondrial intermembrane space assembly machinery40 mutant (Carrie et al, 2010); disrupted in stress responses1 mutant (Gleason et al, 2011); RCC1/UVR8/GEF-like3 mutant (Kühn et al, 2011); and translocase inner membrane subunit23-2-overexpressing and knockout (35S:TIM23-2 and tim23-2) mutants (Wang et al, 2012). For experimental details of the individual microarray studies, see Supplemental Table 1 online.…”

Section: Identification Of a Cis-regulatory Motif In The Promoters Ofmentioning

confidence: 99%

The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis

et al. 2013

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Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain–containing NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana.

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Extensive Rearrangement of the Arabidopsis Mitochondrial Genome Elicits Cellular Conditions for Thermotolerance

Cited by 80 publications

References 36 publications

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis

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