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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
Summary In seed plants, cellulose is synthesized by rosette‐shaped cellulose synthesis complexes (CSCs) that are obligate hetero‐oligomeric, comprising three non‐interchangeable cellulose synthase (CESA) isoforms. The mossPhyscomitrella patenshas rosetteCSCs and sevenCESAs, but its common ancestor with seed plants had rosetteCSCs and a singleCESAgene. Therefore, ifP. patensCSCs are hetero‐oligomeric, thenCSCs of this type evolved convergently in mosses and seed plants. Previous gene knockout and promoter swap experiments showed that PpCESAs from class A (PpCESA3 and PpCESA8) and class B (PpCESA6 and PpCESA7) have non‐redundant functions in secondary cell wall cellulose deposition in leaf midribs, whereas the two members of each class are redundant. Based on these observations, we proposed the hypothesis that the secondary class A and class B PpCESAs associate to form hetero‐oligomericCSCs. Here we show that transcription of secondary class APpCESAs is reduced when secondary class BPpCESAs are knocked out and vice versa, as expected for genes encoding isoforms that occupy distinct positions within the sameCSC. The class A and class B isoforms co‐accumulate in developing gametophores and co‐immunoprecipitate, suggesting that they interact to form a complexin planta. Finally, secondary PpCESAs interact with each other, whereas three of four fail to self‐interact when expressed in two different heterologous systems. These results are consistent with the hypothesis that obligate hetero‐oligomericCSCs evolved independently in mosses and seed plants and we propose the constructive neutral evolution hypothesis as a plausible explanation for convergent evolution of hetero‐oligomericCSCs.
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- Award ID(s):
- 1750359
- 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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