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

Abstract

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. Thus, 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, whereasmore » 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. This article is protected by copyright. All rights reserved.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [4];  [4]; ORCiD logo [2]; ORCiD logo [1]
  1. Department of Biological Sciences University of Rhode Island Kingston RI 02881 USA
  2. Department of Biochemistry and Molecular Biology University of Nevada Reno NV 89557 USA
  3. Wageningen UR Plant Breeding Wageningen University and Research Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands
  4. Department of Biochemistry and Molecular Biology The Pennsylvania State University University Park PA 16802 USA
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1566711
DOE Contract Number:  
SC0001090
Resource Type:
Journal Article
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 99; Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
biofuels (including algae and biomass), bio-inspired, membrane, carbon sequestration, materials and chemistry by design, synthesis (self-assembly)

Citation Formats

Li, Xingxing, Speicher, Tori L., Dees, Dianka C. T., Mansoori, Nasim, McManus, John B., Tien, Ming, Trindade, Luisa M., Wallace, Ian S., and Roberts, Alison W. Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants. United States: N. p., 2019. Web. doi:10.1111/tpj.14366.
Li, Xingxing, Speicher, Tori L., Dees, Dianka C. T., Mansoori, Nasim, McManus, John B., Tien, Ming, Trindade, Luisa M., Wallace, Ian S., & Roberts, Alison W. Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants. United States. doi:10.1111/tpj.14366.
Li, Xingxing, Speicher, Tori L., Dees, Dianka C. T., Mansoori, Nasim, McManus, John B., Tien, Ming, Trindade, Luisa M., Wallace, Ian S., and Roberts, Alison W. Sat . "Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants". United States. doi:10.1111/tpj.14366.
@article{osti_1566711,
title = {Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants},
author = {Li, Xingxing and Speicher, Tori L. and Dees, Dianka C. T. and Mansoori, Nasim and McManus, John B. and Tien, Ming and Trindade, Luisa M. and Wallace, Ian S. and Roberts, Alison W.},
abstractNote = {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. Thus, 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. This article is protected by copyright. All rights reserved.},
doi = {10.1111/tpj.14366},
journal = {The Plant Journal},
issn = {0960-7412},
number = 5,
volume = 99,
place = {United States},
year = {2019},
month = {5}
}

Works referenced in this record:

Visualization of Interactions among bZIP and Rel Family Proteins in Living Cells Using Bimolecular Fluorescence Complementation
journal, April 2002


Collapsed Xylem Phenotype of Arabidopsis Identifies Mutants Deficient in Cellulose Deposition in the Secondary Cell Wall
journal, May 1997

  • Turner, S. R.; Somerville, C. R.
  • The Plant Cell, Vol. 9, Issue 5, p. 689-701
  • DOI: 10.1105/tpc.9.5.689