The Role of Endoplasmic Reticulum Stress Response in Pollen Development and Heat Stress Tolerance

Abstract

Endoplasmic reticulum (ER) stress is defined by a protracted disruption in protein folding and accumulation of unfolded or misfolded proteins in the ER. This accumulation of unfolded proteins can result from excessive demands on the protein folding machinery triggered by environmental and cellular stresses such as nutrient deficiencies, oxidative stress, pathogens, and heat. The cell responds to ER stress by activating a protective pathway termed unfolded protein response (UPR), which comprises cellular mechanisms targeted to maintain cellular homeostasis by increasing the ER’s protein folding capacity. The UPR is especially significant for plants as being sessile requires them to adapt to multiple environmental stresses. While multiple stresses trigger the UPR at the vegetative stage, it appears to be active constitutively in the anthers of unstressed plants. Transcriptome analysis reveals significant upregulation of ER stress-related transcripts in diploid meiocytes and haploid microspores. Interestingly, several ER stress-related genes are specifically upregulated in the sperm cells. The analysis of gene knockout mutants in Arabidopsis has revealed that defects in ER stress response lead to the failure of normal pollen development and enhanced susceptibility of male gametophyte to heat stress conditions. In this mini-review, we provide an overview of the role of ER stress and UPR in pollen development and its protective roles in maintaining male fertility under heat stress conditions.

Circular RNAs Repertoire and Expression Profile during Brassica rapa Pollen Development

“…During pollen development, several mitotic and meiotic cell divisions occur, which involve the expression of a few thousand genes [ 16 , 81 ]. Studies showed that during pollen development, the tapetum endoplasmic reticulum was highly involved in biosynthesis, folding, and secreting proteins [ 82 , 83 ]. For pollen wall formation, lipidic components and polysaccharides are required as tapetum secretes lipid components onto the pollen surface [ 84 , 85 ], or β-glucosidase, which is involved in the regulation of polysaccharide metabolism, downregulated in the sterile floral buds of B. rapa [ 86 ].…”

Insights into the Mechanisms of Heat Priming and Thermotolerance in Tobacco Pollen

“…However, the content of osmotin decreased under severe HS even if pollen previously received priming treatment, suggesting that the protein accumulated under sub-lethal temperatures might be used to cope with a more intense stress. The involvement of proteins of refolding systems besides osmotin, i.e., dehydrins and HSP70, in the acquisition of thermo-tolerance in tobacco pollen was also investigated because the so-called UPR (unfold protein response) is one of the main sensors of thermotolerance at the pollen level [44,45]. Like osmotin, dehydrins can regulate ROS content due to their high content in antioxidant amino acids, such as lysine, histidine, and glycine, and can scavenge ROS through oxidative modification.…”

Holistic insights from pollen omics: co-opting stress-responsive genes and ER-mediated proteostasis for male fertility

“…Furthermore, our comprehensive analyses confirm and extend the idea that ER-stress response is activated in growing tubes ( Fragkostefanakis et al, 2016 ; Liu and Howell, 2016 ) independent of thermoprotection. Mutants of numerous ER-stress response genes ( Supplemental Table S2 ) are either male gametophyte lethal, defective in male transmission, pollen germination, or tube elongation ( Fragkostefanakis et al, 2016 ; Singh et al, 2021 ). The ER-stress response is regulated by ER sensors and ER-associated transcription factors (TFs; see Section “TFs responsive to PT growth are also responsive to other stresses”), though what cues activate it in germinating pollen is unclear.…”

“…We propose five major outcomes when heat stress is sensed at different stages (see Heat 1–5 in Figure 5, A–C ). (1) Microspore development is vulnerable to heat spells in part because the ER UPR is activated in tapetal cells lining the anther chamber in unstressed plants ( Iwata et al, 2008 ; Deng et al, 2016 ; Singh et al, 2021 ). Tapetal cells provide nutrients to the developing pollen, synthesize and secrete compounds for the outer pollen wall, thus disruption of the UPR by heat compromises pollen development and subsequent germination.…”