Abstract The common ancestor of seed plants and mosses contained homo-oligomeric cellulose synthesis complexes (CSCs) composed of identical subunits encoded by a single CELLULOSE SYNTHASE (CESA) gene. Seed plants use different CESA isoforms for primary and secondary cell wall deposition. Both primary and secondary CESAs form hetero-oligomeric CSCs that assemble and function in planta only when all the required isoforms are present. The moss Physcomitrium (Physcomitrella) patens has seven CESA genes that can be grouped into two functionally and phylogenetically distinct classes. Previously, we showed that PpCESA3 and/or PpCESA8 (class A) together with PpCESA6 and/or PpCESA7 (class B) form obligate hetero-oligomeric complexes required for normal secondary cell wall deposition. Here, we show that gametophore morphogenesis requires a member of class A, PpCESA5, and is sustained in the absence of other PpCESA isoforms. PpCESA5 also differs from the other class A PpCESAs as it is able to self-interact and does not co-immunoprecipitate with other PpCESA isoforms. These results are consistent with the hypothesis that homo-oligomeric CSCs containing only PpCESA5 subunits synthesize cellulose required for gametophore morphogenesis. Analysis of mutant phenotypes also revealed that, like secondary cell wall deposition, normal protonemal tip growth requires class B isoforms (PpCESA4 or PpCESA10), along with a class A partner (PpCESA3, PpCESA5, or PpCESA8). Thus, P. patens contains both homo-oligomeric and hetero-oligomeric CSCs.
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Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants
In seed plants, cellulose is synthesized by rosette‐shaped cellulose synthesis complexes (
- Award ID(s):
- 1750359
- NSF-PAR ID:
- 10460401
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 99
- Issue:
- 5
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 862-876
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary The altered carbon assimilation pathway of crassulacean acid metabolism (
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Premise Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (
PTGR s) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD ) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially acceleratePTGR because increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plantPTGR s.Methods We assembled a phylogenetic tree of 451 species with known
PTGR s. We then used comparative phylogenetic methods to detect effects of neo‐polyploidy (within‐genus origins),DNA content, andWGD history onPTGR , and correlated evolution ofPTGR andDNA content.Results Gymnosperms had significantly higher
DNA content and slowerPTGR optima than angiosperms, and theirPTGR andDNA content were negatively correlated. For angiosperms, 89% of model weight favored Ornstein‐Uhlenbeck models with a fasterPTGR optimum for neo‐polyploids, whereasPTGR andDNA content were not correlated. For within‐genus and intraspecific‐cytotype pairs,PTGR s of neo‐polyploids < paleo‐polyploids.Conclusions Genome size increases should negatively affect
PTGR when genetic consequences ofWGD s are minimized, as found in intra‐specific autopolyploids (low heterosis) and gymnosperms (fewWGD s). But in angiosperms, the higherPTGR optimum of neo‐polyploids and non‐negativePTGR ‐DNA content correlation suggest that recurrentWGD s have caused substantialPTGR evolution in a non‐haploid state.
