COPII Sec23 proteins form isoform-specific endoplasmic reticulum exit sites with differential effects on polarized growth

Abstract

COPII, a coat protein complex that forms vesicles on the endoplasmic reticulum (ER), mediates trafficking to the Golgi. While metazoans have few genes encoding each COPII component, plants have expanded these gene families, leading to the hypothesis that plant COPII has functionally diversified. In the moss Physcomitrium (Physcomitrella) patens, the Sec23/24 gene families are each composed of seven genes. Silencing Sec23/24 revealed isoform-specific contributions to polarized growth, with the closely related Sec23D/E and Sec24C/D essential for protonemal development. Focusing on Sec23, we discovered that Sec23D/E mediate ER-to Golgi transport and are essential for tip growth, with Sec23D localizing to presumptive ER exit sites. By contrast, Sec23A,B,C,F, and G are dispensable and do not quantitatively affect ER-to-Golgi trafficking. However, Δsec23abcfg plants exhibited reduced secretion of plasma membrane cargo. Of the four highly expressed protonemal Sec23 genes, Sec23F/G are members of a divergent Sec23 clade specifically retained in land plants. Notably, Sec23G accumulates on ER-associated foci that are significantly larger, do not overlap with, and are independent of Sec23D. While Sec23D/E form ER exit sites and function as bona fide COPII components essential for tip-growing protonemata, Sec23G and the closely related Sec23F have likely functionally diversified, forming separate and independent ER exit sites and participating in Golgi-independent trafficking pathways.

Golgi-Bypass Is a Major Unconventional Route for Translocation to the Plasma Membrane of Non-Apical Membrane Cargoes in Aspergillus nidulans

“…Interestingly, a recent report provided evidence that the assembly and cellular secretion of coronaviruses and other budding viruses employs a direct connection of ERGIC with endosomes, bypassing the passage from Golgi stacks ( Saraste and Prydz, 2021 ). Cargo Golgi-bypass has also been recently speculated in Physcomitrella patens , based on the observation that Sec23 isoforms form distinct and functionally specific COPII/ERes, with some of them affecting ER to Golgi trafficking and polarized growth (i.e., conventional secretion), while others proved unrelated to polarized growth, while affecting specific cargo secretion ( Chang et al, 2021 ). In fact, the multiple isoforms of COPII components present in plants ( Chung et al, 2016 ) and mammals ( Jensen and Schekman, 2011 ) may point to functional diversity, rather than redundancy, related not only to the cargoes selected but also the trafficking route followed after ER-exit.…”

“…Other reports have shown that Sec24 isoforms (paralogs) are selective towards distinct cargoes ( Roberg et al, 1999 ; Miller et al, 2002 ) or are non-uniformly distributed to ERes in S. cerevisiae ( Iwasaki et al, 2015 ). In addition, in the moss Physcomitrella patens , COPII Sec23 isoforms have been shown to form specific ER-exit sites with differential effects on polarized growth ( Chang et al, 2021 ). A hypothesis that cargo identity may define the formation of distinct COPII complexes and vesicle populations during plant development and in response to stress has also been proposed ( Tanaka et al, 2013 ; Chung et al, 2016 ).…”

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.…”

“…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 ]. The knockout of the Sec23 d gene suppressed the protein transportation between ER and Golgi and protein secretion in the mutant plants, leading to ER morphology defects and ER stress [ 60 ].…”

“…In Physcomitrium patens , Sec23D is localized in the presumptive ER-exit sites [ 60 ]. The knockout of the Sec23 d gene suppressed the protein transportation between ER and Golgi and protein secretion in the mutant plants, leading to ER morphology defects and ER stress [ 60 ]. In A.thaliana , Sar1A is also localized in ER-exit sites [ 63 ].…”