COPII genes SEC31A/B are essential for gametogenesis and interchangeable in pollen development in Arabidopsis

Abstract

In eukaryotes, coat protein complex II (COPII) vesicles mediate anterograde traffic from the endoplasmic reticulum to the Golgi apparatus. Compared to yeasts, plants have multiple COPII coat proteins; however, the functional diversity among them is less well understood. SEC31A and SEC31B are outer coat proteins found in COPII vesicles in Arabidopsis. In this study, we explored the function of SEC31A and compared it with that of SEC31B from various perspectives. SEC31A was widely expressed, but at a significantly lower level than SEC31B. SEC31A-mCherry and SEC31B-GFP exhibited a high co-localization rate in pollen, but a lower rate in growing pollen tubes. The sec31a single mutant exhibited normal growth. SEC31A expression driven by the SEC31B promoter rescued the pollen abortion and infertility observed in sec31b. A sec31a-sec31b double mutant was unavailable due to lethality of the sec31asec31b gametophyte. Transmission electron microscopy revealed that one quarter of male gametogenesis was arrested at the uninuclear microspore stage, while confocal laser scanning microscopy showed that 1/4 female gametophyte development was suspended at the functional megaspore stage in sec31a-1/+sec31b-3/+ plants. Our study highlights the essential role of SEC31A/B in gametogenesis and their interchangeable functions in pollen development.

COPII vesicles in plant autophagy and endomembrane trafficking

“…2 and Table 1). The inner coat AtSec23/ 24s and outer coat Sec31s are mostly studied in regard to their functions in ER-Golgi integrity, sepal cell size regulation, pollen development and gametogenesis [50][51][52][53][54][55][56][57]. AtSec24a is important for maintaining ER morphology, whereby, in missense sec24a mutants, the normal ER-Golgi interface is disrupted with aberrant clustering of ER/Golgi-derived membrane aggregates, whereas knockout of AtSec24a is seedling lethal [50,51].…”

“…Studies of gametogenesis further suggested incomplete overlapping functions of the three AtSec24s for the transportation of unidentified cargo proteins for pollen development or female gametogenesis [53,54]. In connection with the findings of AtSec23 and AtSec31 homologs functioning specifically in pollen development, it would be of great interest to reconsider the pairing and cooperation of distinct COPII homologs in the formation of specific COPII vesicle populations for plant development in different stages and tissues [55][56][57]. With the development of transcriptomics and proteomics approaches, a revisit to the 'unknown factors' in past studies may result to novel discoveries.…”

“…In contrast to the well-characterized core autophagic machineries in yeast and mammals, plants contain not only counterparts of these ATG proteins, but also additional factors unique to higher plants, highlighting the regulation of autophagosomes in sessile lives Not required for normal growth, play interchangeable roles with Sec31b in pollen development [56] responding to environmental stresses [21,[65][66][67][68]. Plant autophagy regulators are discovered during the investigation of how the secretory pathway crosstalks with the autophagic flux or regulates autophagosome biogenesis [23,69].…”

Critical Determinants in ER-Golgi Trafficking of Enzymes Involved in Glycosylation

“…The Multiple paralogs of COPII protein components were also discovered in plants [ 59 ]. The expression pattern, subcellular localization, and function of the COPII protein paralogs showed a significant difference [ 60 , 61 , 62 , 63 ]. SEC23A/SEC23D [ 64 ], SEC31A/B [ 61 , 65 ] and Sar1B/C [ 62 ] had been reported to be required in pollen development.…”

“…The expression pattern, subcellular localization, and function of the COPII protein paralogs showed a significant difference [ 60 , 61 , 62 , 63 ]. SEC23A/SEC23D [ 64 ], SEC31A/B [ 61 , 65 ] and Sar1B/C [ 62 ] had been reported to be required in pollen development. In Physcomitrium patens , Sec23D is localized in the presumptive ER-exit sites [ 60 ].…”