Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen

Abstract

Background Cytoplasmic male sterility (CMS) is a maternally inherited failure to produce functional pollen that most commonly results from expression of novel, chimeric mitochondrial genes. In Zea mays, cytoplasmic male sterility type S (CMS-S) is characterized by the collapse of immature, bi-cellular pollen. Molecular and cellular features of developing CMS-S and normal (N) cytoplasm pollen were compared to determine the role of mitochondria in these differing developmental fates. Results Terminal deoxynucleotidyl transferase dUTP nick end labeling revealed both chromatin and nuclear fragmentation in the collapsed CMS-S pollen, demonstrating a programmed cell death (PCD) event sharing morphological features with mitochondria-signaled apoptosis in animals. Maize plants expressing mitochondria-targeted green fluorescent protein (GFP) demonstrated dynamic changes in mitochondrial morphology and association with actin filaments through the course of N-cytoplasm pollen development, whereas mitochondrial targeting of GFP was lost and actin filaments were disorganized in developing CMS-S pollen. Immunoblotting revealed significant developmental regulation of mitochondrial biogenesis in both CMS-S and N mito-types. Nuclear and mitochondrial genome encoded components of the cytochrome respiratory pathway and ATP synthase were of low abundance at the microspore stage, but microspores accumulated abundant nuclear-encoded alternative oxidase (AOX). Cytochrome pathway and ATP synthase components accumulated whereas AOX levels declined during the maturation of N bi-cellular pollen. Increased abundance of cytochrome pathway components and declining AOX also characterized collapsed CMS-S pollen. The accumulation and robust RNA editing of mitochondrial transcripts implicated translational or post-translational control for the developmentally regulated accumulation of mitochondria-encoded proteins in both mito-types. Conclusions CMS-S pollen collapse is a PCD event coincident with developmentally programmed mitochondrial events including the accumulation of mitochondrial respiratory proteins and declining protection against mitochondrial generation of reactive oxygen species.

Transcriptomics reveals a core transcriptional network of K-type cytoplasmic male sterility microspore abortion in wheat (Triticum aestivum L.)

“…In addition, the upregulation of alternative oxidase (AOX) expression may be caused by the inhibition of cytochrome pathway, this is consistent with Karen's research [97]. Previous studies have shown that defects in the TCA cycle may also lead to producing excessive amounts of ROS.…”

The mitochondrialorf117Shagene desynchronizes pollen development and causes pollen abortion in the Arabidopsis Sha CMS

“…However, the coincidence between the heterogeneity of mitochondria volumes with the pollen death heterogenous timing leads us to hypothesize that mitochondria swelling likely reflects a late phase in the process of pollen abortion. No mitochondria swelling in pollen was reported in the gametophytic S-CMS of maize after mitochondria-targeted GFP imaging (Chamusco et al, 2022), and mitochondrial morphology was not described in the HL-CMS of rice, to our knowledge.…”

“…However, the coincidence between the heterogeneity of mitochondria volumes with the pollen death heterogenous timing leads us to hypothesize that mitochondria swelling likely reflects a late phase in the process of pollen abortion. No mitochondria swelling in pollen was reported in the gametophytic S-CMS of maize after mitochondria-targeted GFP imaging (Chamusco et al ., 2022), and mitochondrial morphology was not described in the HL-CMS of rice, to our knowledge. However, changes in mitochondrial morphology were reported from electron microscopy observations in the tapetal cells of sporophytic sunflower PET1-CMS (Horner, 1977), rapeseed Ogura CMS (González-Melendi et al ., 2008), soybean CMS (Smith et al ., 2002), and of thermosensitive genic-male sterility of rice (Ku et al ., 2003) and in pollen tubes experiencing the Papaver rhoeas self-incompatibility response (Geitmann et al ., 2004), supporting the view that it is a convergent step in diverse cell death processes.…”

Early detection of late blight in potato by whole‐plant redox imaging

“…roGFP‐based biosensors are effective tools for exploring redox dynamics in subcellular compartments at high spatiotemporal resolution in plants (Bratt et al., 2016; Gutscher et al., 2008; Jiang et al., 2006; Lampl et al., 2022; Meyer, 2008; Meyer & Dick, 2010; Nietzel et al., 2019; Schwarzländer et al., 2016; Ugalde et al., 2021; Ugalde et al., 2022). Genetically encoded biosensors have also been introduced into crop plants, including potato (Chamusco et al., 2022; Hipsch et al., 2021; Huang et al., 2014; Rattanawong et al., 2021), and spatially resolved mapping of stress‐induced long‐term redox perturbations has recently been demonstrated by whole‐plant imaging of potato plants expressing roGFP2 in their chloroplasts (Hipsch et al., 2021). Additionally, in potato plants infected with the potato virus Y, chloroplast‐targeted roGFP2 has been used to demonstrate the role of chloroplast redox state in SA‐independent cell death signaling and SA‐dependent HR (Lukan et al., 2023).…”