Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants

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

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The secondary cell walls of tracheary elements and fibers are rich in cellulose microfibrils that are helically oriented and laterally aggregated. Support cells within the leaf midribs of mosses deposit cellulose-rich secondary cell walls, but their biosynthesis and microfibril organization have not been examined. Although the Cellulose Synthase (CESA) gene families of mosses and seed plants diversified independently, CESA knockout analysis in the moss Physcomitrella patens revealed parallels with Arabidopsis (Arabidopsis thaliana) in CESA functional specialization, with roles for both subfunctionalization and neofunctionalization. The similarities include regulatory uncoupling of the CESAs that synthesize primary and secondary cell walls, a requirement for two or more functionally distinct CESA isoforms for secondary cell wall synthesis, interchangeability of some primary and secondary CESAs, and some CESA redundancy. The cellulose-deficient midribs of ppcesa3/8 knockouts provided negative controls for the structural characterization of stereid secondary cell walls in wild type P. patens. Sum frequency generation spectra collected from midribs were consistent with cellulose microfibril aggregation, and polarization microscopy revealed helical microfibril orientation only in wild type leaves. Thus, stereid secondary walls are structurally distinct from primary cell walls, and they share structural characteristics with the secondary walls of tracheary elements and fibers. We propose a mechanism for the convergent evolution of secondary walls in which the deposition of aggregated and helically oriented microfibrils is coupled to rapid and highly localized cellulose synthesis enabled by regulatory uncoupling from primary wall synthesis.

Original languageEnglish (US)
Pages (from-to)210-222
Number of pages13
JournalPlant physiology
Volume175
Issue number1
DOIs
StatePublished - Sep 2017

Fingerprint

cellulose synthase
Bryophyta
Microfibrils
Spermatophytina
Cell Wall
mosses and liverworts
Seeds
Protein Isoforms
Cellulose
cell walls
cellulose
tracheary elements
Physcomitrella patens
Arabidopsis
synthesis
Bryopsida
Polarization Microscopy
convergent evolution
leaves
microscopy

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Norris, J. H., Li, X., Huang, S., Van De Meene, A. M. L., Tran, M. L., Killeavy, E., ... Roberts, A. W. (2017). Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants. Plant physiology, 175(1), 210-222. https://doi.org/10.1104/pp.17.00885
Norris, Joanna H. ; Li, Xingxing ; Huang, Shixin ; Van De Meene, Allison M.L. ; Tran, Mai L. ; Killeavy, Erin ; Chaves, Arielle M. ; Mallon, Bailey ; Mercure, Danielle ; Tan, Hwei Ting ; Burton, Rachel A. ; Doblin, Monika S. ; Kim, Seong H. ; Roberts, Alison W. / Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants. In: Plant physiology. 2017 ; Vol. 175, No. 1. pp. 210-222.
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Norris, JH, Li, X, Huang, S, Van De Meene, AML, Tran, ML, Killeavy, E, Chaves, AM, Mallon, B, Mercure, D, Tan, HT, Burton, RA, Doblin, MS, Kim, SH & Roberts, AW 2017, 'Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants', Plant physiology, vol. 175, no. 1, pp. 210-222. https://doi.org/10.1104/pp.17.00885

Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants. / Norris, Joanna H.; Li, Xingxing; Huang, Shixin; Van De Meene, Allison M.L.; Tran, Mai L.; Killeavy, Erin; Chaves, Arielle M.; Mallon, Bailey; Mercure, Danielle; Tan, Hwei Ting; Burton, Rachel A.; Doblin, Monika S.; Kim, Seong H.; Roberts, Alison W.

In: Plant physiology, Vol. 175, No. 1, 09.2017, p. 210-222.

Research output: Contribution to journalArticle

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AU - Norris, Joanna H.

AU - Li, Xingxing

AU - Huang, Shixin

AU - Van De Meene, Allison M.L.

AU - Tran, Mai L.

AU - Killeavy, Erin

AU - Chaves, Arielle M.

AU - Mallon, Bailey

AU - Mercure, Danielle

AU - Tan, Hwei Ting

AU - Burton, Rachel A.

AU - Doblin, Monika S.

AU - Kim, Seong H.

AU - Roberts, Alison W.

PY - 2017/9

Y1 - 2017/9

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Norris JH, Li X, Huang S, Van De Meene AML, Tran ML, Killeavy E et al. Functional specialization of cellulose synthase isoforms in a moss shows parallels with seed plants. Plant physiology. 2017 Sep;175(1):210-222. https://doi.org/10.1104/pp.17.00885