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Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants
Author(s) -
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.
Publication year - 2019
Publication title -
the plant journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.058
H-Index - 269
eISSN - 1365-313X
pISSN - 0960-7412
DOI - 10.1111/tpj.14366
Subject(s) - convergent evolution , cellulose , materials science , botany , polymer science , chemical engineering , chemistry , biology , organic chemistry , biochemistry , engineering , phylogenetics , gene
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.