Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants

Norris, Joanna H.; Li, Xingxing; Huang, Shixin; Meene, Allison van de; Tran, Mai L.; Killeavy, Erin E.; Chaves, Arielle M.; Mallon, Bailey; Mercure, Danielle; Tan, Hwei-Ting; Burton, Rachel A.; Doblin, Monika S.; Kim, Seong H.; Roberts, Alison W.

doi:10.1104/pp.17.00885

Cited by 29 publications

(54 citation statements)

References 62 publications

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“…The biosynthesis of secondary walls necessitates the coordinated expression of genes in the biosynthetic pathways of cellulose, xylan, glucomannan and lignin, which is mediated by a transcriptional network encompassing a group of secondary wall NAC and MYB master transcriptional switches and their downstream targets (Zhong & Ye, ). Although the moss Physcomitrella patens , a nonvascular plant species, has no lignified secondary walls, its genome harbors close homologs of most secondary wall biosynthetic genes (Liepman et al ., ; Xu et al ., ; Kulkarni et al ., ; Haghighat et al ., ; Norris et al ., ). It is therefore very likely that vascular plants co‐opted these genes, via gene duplication and functional diversification, to synthesize secondary walls in the first‐evolved water‐conducting tracheids.…”

Section: Introductionmentioning

confidence: 97%

Secondary cell wall biosynthesis

2018

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Contents Summary1703I.Introduction1703II.Cellulose biosynthesis1705III.Xylan biosynthesis1709IV.Glucomannan biosynthesis1713V.Lignin biosynthesis1714VI.Concluding remarks1717Acknowledgements1717References1717 Summary Secondary walls are synthesized in specialized cells, such as tracheary elements and fibers, and their remarkable strength and rigidity provide strong mechanical support to the cells and the plant body. The main components of secondary walls are cellulose, xylan, glucomannan and lignin. Biochemical, molecular and genetic studies have led to the discovery of most of the genes involved in the biosynthesis of secondary wall components. Cellulose is synthesized by cellulose synthase complexes in the plasma membrane and the recent success of in vitro synthesis of cellulose microfibrils by a single recombinant cellulose synthase isoform reconstituted into proteoliposomes opens new doors to further investigate the structure and functions of cellulose synthase complexes. Most genes involved in the glycosyl backbone synthesis, glycosyl substitutions and acetylation of xylan and glucomannan have been genetically characterized and the biochemical properties of some of their encoded enzymes have been investigated. The genes and their encoded enzymes participating in monolignol biosynthesis and modification have been extensively studied both genetically and biochemically. A full understanding of how secondary wall components are synthesized will ultimately enable us to produce plants with custom‐designed secondary wall composition tailored to diverse applications.

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Section: Introductionmentioning

confidence: 97%

Secondary cell wall biosynthesis

2018

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“…Consequently, the secondary cell wall provides structural support for the 58 5 cellulose in secondary cell walls . However, a recent analysis of CESA proteins 84 from the moss Physcomitrella suggests that separate CESAs are required for both primary and 85 secondary cell walls, but these CESA proteins do not form separate classes and it seems likely a 86 single CESA class is sufficient to make cellulose (Norris et al, 2017). This implies that the 87 requirement for multiple CESA in higher plants is not essential for cellulose synthesis per se, but 88 maybe a means of fine-tuning the regulation of cellulose synthesis in response to various external 89 cues.…”

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Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis

et al. 2018

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“…Recently we have shown that four PpCESAs, two members of class A (PpCESA3 or PpCESA8) and two members of class B (PpCESA6 or PpCESA7), participate in cellulose deposition in stereid cell secondary cell walls in P. patens leaf midribs (Norris et al ., ). Although single knockout (KO) mutants had little or no mutant phenotype, both ppcesa3/8 KO and ppcesa6/7 KO lines had cellulose‐deficient midribs, suggesting that PpCESA3 and PpCESA8 from class A are redundant and that their role is distinct from that of PpCESA6 and PpCESA7, which constitute a second redundant pair from class B (Norris et al ., ). This finding was supported by promoter swap experiments showing that ppcesa3/ 8KO could be rescued by PpCESA8pro:PpCESA3 or PpCESA8pro:PpCESA8 , but not P pCESA8pro:PpCESA7 (Norris et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…Although single knockout (KO) mutants had little or no mutant phenotype, both ppcesa3/8 KO and ppcesa6/7 KO lines had cellulose‐deficient midribs, suggesting that PpCESA3 and PpCESA8 from class A are redundant and that their role is distinct from that of PpCESA6 and PpCESA7, which constitute a second redundant pair from class B (Norris et al ., ). This finding was supported by promoter swap experiments showing that ppcesa3/ 8KO could be rescued by PpCESA8pro:PpCESA3 or PpCESA8pro:PpCESA8 , but not P pCESA8pro:PpCESA7 (Norris et al ., ). These data are consistent with the hypothesis that CSCs responsible for secondary cell wall deposition in P. patens are hetero‐oligomeric with some positions that can be occupied by PpCESA3 or PpCESA8 (class A secondary PpCESAs) and others that can be occupied by PpCESA6 or PpCESA7 (class B secondary PpCESAs).…”

Section: Introductionmentioning

confidence: 97%

“…These data are consistent with the hypothesis that CSCs responsible for secondary cell wall deposition in P. patens are hetero‐oligomeric with some positions that can be occupied by PpCESA3 or PpCESA8 (class A secondary PpCESAs) and others that can be occupied by PpCESA6 or PpCESA7 (class B secondary PpCESAs). If this hypothesis is correct, then hetero‐oligomeric CSCs evolved independently in mosses and seed plants (Norris et al ., ). However, it has not been demonstrated that PpCESA3, PpCESA8, PpCESA6 and PpCESA7 reside in the same complex.…”

Section: Introductionmentioning

confidence: 97%

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Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

Speicher

Dees

et al. 2019

The Plant Journal

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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 moss Physcomitrella patens has rosette CSCs and seven CESAs, but its common ancestor with seed plants had rosette CSCs and a single CESA gene. Therefore, if P. patens CSCs are hetero‐oligomeric, then CSCs 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‐oligomeric CSCs. Here we show that transcription of secondary class A PpCESAs is reduced when secondary class B PpCESAs are knocked out and vice versa, as expected for genes encoding isoforms that occupy distinct positions within the same CSC. The class A and class B isoforms co‐accumulate in developing gametophores and co‐immunoprecipitate, suggesting that they interact to form a complex in 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‐oligomeric CSCs evolved independently in mosses and seed plants and we propose the constructive neutral evolution hypothesis as a plausible explanation for convergent evolution of hetero‐oligomeric CSCs.

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Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants

Cited by 29 publications

References 62 publications

Secondary cell wall biosynthesis

Secondary cell wall biosynthesis

Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis

Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants

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