Abstract

Mitochondria play key roles in cellular-energy metabolism and are vital for plant-life, such as for successful germination and early-seedling establishment. Most mitochondria contain their own genetic system (mtDNA, mitogenome), with an intrinsic protein-synthesis machinery. Although the challenges of maintaining prokaryotic-type structures and functions are common to Eukarya, land plants possess some of the most complex organelle composition of all known organisms. Angiosperms mtDNAs are characteristically the largest and least gene-dense among the eukaryotes. They often contain highly-variable intergenic regions of endogenous or foreign origins and undergo frequent recombination events, which result in different mtDNA configurations, even between closely-related species. The expression of the mitogenome in angiosperms involves extensive mtRNA processing steps, including numerous editing and splicing events. Why do land-plant’s mitochondria have to be so complex? The answer to this remains a matter of speculation. We propose that this complexity may have arisen throughout the terrestrialization of plants, as a means to control embryonic mitochondrial functions —a critical adaptive trait to optimize seed germination. The unique characteristics of plant mtDNA may play pivotal roles in the nuclear-regulation of organellar biogenesis and metabolism, possibly to control embryos quiescence or dormancy, essential determinants for the establishment of viable plantlets that can survive post-germination.

Highlights

  • We speculate that large organellar genomes with a complex mode of gene expression, in particular at the posttranscriptional level, allow plants to tightly control the respiratory-mediated functions, and to minimize cellular metabolism, until environmental conditions are favorable for germination

  • Temperature- and tissue-depended splicing have been shown for mtRNAs during germination and early seedling establishment [46,133,134], further signifying the importance of group II intron splicing as a means to regulate the expression of mitochondrial genes during these critical stages in land plant life

  • While mitochondria found in the embryonic cells of animals remain fully active throughout development, the mitochondria of embryos in flowering plants undergo a dedifferentiation during seed maturation

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Summary

Overview

The evolution of land plants from a green algal ancestor, about half a billion years ago [1,2], was a remarkable event in the history of life on earth. From a botanical point of view, functional and molecular analysis of angiosperm mitochondria provide important insights into the evolution of land plants, nuclear-cytoplasmic interactions, and mitochondria-related physiological traits [16] These features are expected to be highly valuable for future agriculture and crop improvement, especially under suboptimal growth conditions. Our focus for this manuscript is studies aimed at understanding the evolutionary selection pressures that have shaped the angiosperms mitogenome organization and the intricacy of their gene expression designs We speculate that this organellar complexity relates to the necessity of land plants to regulate germination and to maintain that their offspring are quiescent or dormant until environmental conditions become favorable for their germination. Embryogenesis, Seed Maturation, and Germination Rely on Mitochondria Functions and Cellular Metabolism

Seed as a Major Adaptation of Plants to Life on Land
Mitochondria Biogenesis and Respiratory Reactivation during Seed Germination
Organization of Angiosperm Mitochondrial Genomes
RNA Editing Plays a Key Role in the Regulation of mtDNA Expression
Angiosperm Mitochondria Gene Copy Numbers
Findings
Concluding Remarks
Full Text
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