Organellar protein multi-functionality and phenotypic plasticity in plants

Abstract

With the increasing impact of climate instability on agricultural and ecological systems has come a heightened sense of urgency to understand plant adaptation mechanisms in more detail. Plant species have a remarkable ability to disperse their progeny to a wide range of environments, demonstrating extraordinary resiliency mechanisms that incorporate epigenetics and transgenerational stability. Surprisingly, some of the underlying versatility of plants to adapt to abiotic and biotic stress emerges from the neofunctionalization of organelles and organellar proteins. We describe evidence of possible plastid specialization and multi-functional organellar protein features that serve to enhance plant phenotypic plasticity. These features appear to rely on, for example, spatio-temporal regulation of plastid composition, and unusual interorganellar protein targeting and retrograde signalling features that facilitate multi-functionalization. Although we report in detail on three such specializations, involving MSH1, WHIRLY1 and CUE1 proteins in Arabidopsis, there is ample reason to believe that these represent only a fraction of what is yet to be discovered as we begin to elaborate cross-species diversity. Recent observations suggest that plant proteins previously defined in one context may soon be rediscovered in new roles and that much more detailed investigation of proteins that show subcellular multi-targeting may be warranted. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.

Keywords: WHIRLY; abiotic and biotic stress; epigenetics; retrograde signalling.

Figure 1.

The MSH1 effect outlined in Arabidopsis. Plastidic and mitochondrial outcomes following MSH1 suppression and selection. Enhanced illegitimate recombination within the mitochondrial genome leads to substoichiometric shifting and expression of a male sterility trait. Lack of pollination in a CMS line can lead to low-frequency reversion to fertility, similarly involving MSH1 effects and mitochondrial subgenomic shifting. Depletion of MSH1 from the sensory plastid produces a variable stress-response phenotype that conditions transgenerational memory and enhanced stress tolerance. Memory line crossing or grafting with wild-type (WT) produces enhanced fitness traits (Epi). These effects are recapitulated across plant species, suggesting a role for MSH1 in plant adaptation.

Figure 2.

A simplified model of organellar influences on plant phenotypic plasticity. Stress-associated suppression of MSH1 expression alters conditions within the sensory plastid of epidermal and vascular parenchyma cells [55]. These changes involve at least two retrograde signalling pathways to the nucleus, one including redox and calcium signalling [53] and the other tocopherol-mediated modulation of the PAP phosphonucleotide as a mediator of miRNA regulation [55,109]. Nuclear response to sensory plastid perturbation includes genome-wide cytosine methylation repatterning and altered expression of integrated stress response networks. Transgenerational memory induced by MSH1 suppression gives rise, through crossing or grafting, to progeny with markedly enhanced growth vigour and resilience phenotypes [77,79,87,89]. WHY1 is localized to both mesophyll chloroplasts and sensory plastids [53], whereas WHY2 targets to mitochondria. However, WHY1 is distinctive in its apparent ability to transit back to the nucleus following plastid processing of the presequence [98]. This transiting allows WHY1 to function as a transcription factor in regulating stress responses. CUE1, a sensory plastid-specific PEP translocator, participates in tocopherol biosynthesis and the PAP-mediated retrograde signalling to regulate miRNA stability in the nucleus.