Contribution of Massive Mitochondrial Fusion and Subsequent Fission in the Plant Life Cycle to the Integrity of the Mitochondrion and Its Genome

Abstract

Plant mitochondria have large genomes to house a small number of key genes. Most mitochondria do not contain a whole genome. Despite these latter characteristics, the mitochondrial genome is faithfully maternally inherited. To maintain the mitochondrial genes—so important for energy production—the fusion and fission of mitochondria are critical. Fission in plants is better understood than fusion, with the dynamin-related proteins (DRP 3A and 3B) driving the constriction of the mitochondrion. How the endoplasmic reticulum and the cytoskeleton are linked to the fission process is not yet fully understood. The fusion mechanism is less well understood, as obvious orthologues are not present. However, there is a recently described gene, MIRO2, that appears to have a significant role, as does the ER and cytoskeleton. Massive mitochondrial fusion (MMF or hyperfusion) plays a significant role in plants. MMF occurs at critical times of the life cycle, prior to flowering, in the enlarging zygote and at germination, mixing the cells’ mitochondrial population—the so-called “discontinuous whole”. MMF in particular aids genome repair, the conservation of critical genes and possibly gives an energy boost to important stages of the life cycle. MMF is also important in plant regeneration, an important component of plant biotechnology.

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

“…However, as noted above, mitochondria and plastids both possess low genome copy numbers in the SAM and/or reproductive tissues [35][36][37][38], presenting similar potential for physical bottlenecks. One key difference between the two types of organelles is that mitochondria can experience both full and transient fusion events over the plant life cycle allowing for genetic exchange, whereas plastids rarely if ever fuse [12,[75][76][77][78][79].…”

Altered collective mitochondrial dynamics in an Arabidopsis msh1 mutant compromising organelle DNA maintenance

“…Processes of mtDNA exchange and recombination are essential to maintain this diverse structure (Bellaoui et al, 1998;Arrieta-Montiel et al, 2009;Davila et al, 2011;Gualberto and Newton, 2017), with mtDNA sharing through the population of mitochondria constituting a 'discontinuous whole' (Logan, 2006a). Such sharing and recombination is inherently shaped and limited by the physical behaviour of organelles in the cell (Belliard, Vedel and Pelletier, 1979;Lonsdale et al, 1988;Gualberto and Newton, 2017;Aryaman et al, 2019;Johnston, 2019;Rose, 2021). In the shoot apical meristem (SAM), a cage-like mitochondrial network has been observed to form (Seguí-Simarro and Staehelin, 2009), in contrast to the largely individual mitochondria observed in other tissues.…”

“…In the shoot apical meristem (SAM), a cage-like mitochondrial network has been observed to form (Seguí-Simarro and Staehelin, 2009), in contrast to the largely individual mitochondria observed in other tissues. This network structure allows mtDNA mixing and may facilitate recombination (Edwards et al, 2021;Rose, 2021). In conjunction with this physical change, relative expression of MSH1 is particularly high in the SAM, which may both assist with maintenance and support germline mtDNA segregation through gene conversion as an evolutionary priority (Schmid et al, 2005;Edwards et al, 2021).…”

“…Mitochondria need to be physically proximal to allow membrane fusion and mixing of contents including mitochondrial DNA (mtDNA) (Arimura et al, 2004;Sheahan, McCurdy and Rose, 2005;Rose, 2021). In addition to this exchange, mitochondrial proximity facilitates metabolic exchange and mitochondrial quality control, a process reliant on cycles of fission and fusion, key for maintaining a healthy chondriome (Jones, 1986;Karbowski and Youle, 2003;Arimura et al, 2004;Logan, 2006a;Takanashi et al, 2006;Twig et al, 2008;Liu et al, 2009;Figge et al, 2012;Shutt and McBride, 2013;Agrawal, Pekkurnaz and Koslover, 2018).…”

Altered collective mitochondrial dynamics in the Arabidopsismsh1mutant compromising organelle DNA maintenance

“…Such sharing and recombination is inherently shaped and limited by the physical behaviour of organelles in the cell ( Belliard et al , 1979 ; Lonsdale et al , 1988 ; Gualberto and Newton, 2017 ; Aryaman et al , 2019 ; Johnston, 2019 ; Rose, 2021 ). In order for this sharing to occur, mitochondria must physically meet and exchange contents—so the genetic structure of the mtDNA population is inherently controlled by the physical dynamics of the mitochondrial compartments.…”