Mitochondrial dynamics and segregation during the asymmetric division of Arabidopsis zygotes

Abstract

The zygote is the first cell of a multicellular organism. In most angiosperms, the zygote divides asymmetrically to produce an embryo-precursor apical cell and a supporting basal cell. Zygotic division should properly segregate symbiotic organelles, because they cannot be synthesized de novo. In this study, we revealed the real-time dynamics of the principle source of ATP biogenesis, mitochondria, in Arabidopsis thaliana zygotes using live-cell observations and image quantifications. In the zygote, the mitochondria formed the extended structure associated with the longitudinal array of actin filaments (F-actins) and were polarly distributed along the apical–basal axis. The mitochondria were then temporally fragmented during zygotic division, and the resulting apical cells inherited mitochondria at higher concentration compared to the basal cells. Further observation of postembryonic organs showed that these mitochondrial behaviours are characteristic of the zygote. Overall, our results showed that the zygote has spatiotemporal regulation that unequally distributes the mitochondria.

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

“…The egg cell has a mix of punctate and tubular mitochondria. However, the zygote has extremely long tubular mitochondria, most likely due to MMF [ 83 ]. These long tubular mitochondria form in association with long F-actin filaments.…”

“…Nucleoids are present in 90% of the promitochondria. It is feasible that the MMF that occurs in the SAM [ 10 , 82 ] and in the zygote [ 83 ] contributes to the nucleoid content being less heterogeneous in the promitochondrial population. During germination, there is MMF in the form of tubuloreticular mitochondria that surround the nucleus, similar to what occurs in the SAM.…”

“…This means that it provides an important opportunity for all the subgenomes to interact for recombination and DNA repair for the next generation. What is known currently is that MMF occurs in the SAM [ 10 , 82 ] where flowering is initiated, in the zygote [ 83 ] and in germination [ 86 ], which are key points in the life cycle. This is not to say that the fusion/fission cycle involving few mitochondria is not unimportant in the cell cycle, cell development and the functioning of the cell.…”

TheArabidopsisembryo as a quantifiable model for studying pattern formation

“…Achievement of these goals became feasible with application of an in vitro ovule cultivation system allowing tracking of early embryogenesis events (Gooh et al, 2015). Livecell imaging was also successfully used to study mitochondria, vacuole and cytoskeleton organisation of in vitro cultivated Arabidopsis zygotes (Kimata et al, 2016;Kimata et al, 2019;Kimata et al, 2020). Although these live-imaging techniques provide a unique opportunity to visualise processes occurring in the embryo enclosed into developing seed, they are not without their own challenges.…”

“…Asymmetric cell divisions, o en considered formative divisions, are key to tissue formation, and require that resulting daughter cells not only differ in morphology, but most importantly possess distinct identities (Scheres & Benfey, 1999). Acquisition of different identities is preceded by establishment of cellular polarity reflected in segregation of subcellular components such as hormones, mRNA, proteins and organelles between two daughter cells, and can be influenced by both intrinsic and extrinsic mechanisms (Dong et al, 2009;Kimata et al, 2016;Kimata et al, 2019;Kimata et al, 2020). Intrinsic regulation relies on activation of cell type-specific transcriptional networks, while extrinsic control is determined by cellular environment and involves cell-to-cell communication through different mobile molecular signals such as short miRNA, short peptides, hormones, as well as mechanical cues (Heisler et al, 2010;Schlereth et al, 2010).…”