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

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.

doi:10.1111/tpj.14366

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

Journal Article · 25 May 2019 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.14366 · OSTI ID:1515787

Li, Xingxing ^[1]; Speicher, Tori L. ^[2]; Dees, Dianka C. T. ^[3]; Mansoori, Nasim ^[3]; McManus, John B. ^[4]; Tien, Ming ^[4]; Trindade, Luisa M. ^[4];

^[2];

^[1]

Department of Biological Sciences University of Rhode Island Kingston RI 02881 USA
Department of Biochemistry and Molecular Biology University of Nevada Reno NV 89557 USA
Wageningen UR Plant Breeding Wageningen University and Research Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands
Department of Biochemistry and Molecular Biology The Pennsylvania State University University Park PA 16802 USA

Summary In seed plants, cellulose is synthesized by rosette‐shaped cellulose synthesis complexes ( CSC s) that are obligate hetero‐oligomeric, comprising three non‐interchangeable cellulose synthase ( CESA ) isoforms. The moss Physcomitrella patens has rosette CSC s and seven CESA s, but its common ancestor with seed plants had rosette CSC s and a single CESA gene. Therefore, if P. patens CSC s are hetero‐oligomeric, then CSC s of this type evolved convergently in mosses and seed plants. Previous gene knockout and promoter swap experiments showed that Pp CESA s from class A (Pp CESA 3 and Pp CESA 8) and class B (Pp CESA 6 and Pp CESA 7) 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 Pp CESA s associate to form hetero‐oligomeric CSC s. Here we show that transcription of secondary class A Pp CESA s is reduced when secondary class B Pp CESA s 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 Pp CESA s 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 CSC s 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 CSC s.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐SC0001090

OSTI ID:: 1515787

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Vol. 99 Journal Issue: 5; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 6 works

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