Evolutionary divergence of β–expansin structure and function in grasses parallels emergence of distinctive primary cell wall traits

• Published in: The Plant journal : for cell and molecular biology Vol. 81; no. 1
• Main Authors: Sampedro, Javier, Guttman, Mara, Li, Lian‐Chao, Cosgrove, Daniel J.
• Format: Journal Article
• Language: English
• Published: United Kingdom Wiley-Blackwell 27.11.2014
• ISSN: 0960-7412; 1365-313X

Summary Expansins are wall‐loosening proteins that promote the extension of primary cell walls without the hydrolysis of major structural components. Previously, proteins from the <styled-content style='fixed-case'>EXPA</styled-content> (α–expansin) family were found to loosen eudicot cell walls but to be less effective on grass cell walls, whereas the reverse pattern was found for <styled-content style='fixed-case'>EXPB</styled-content> (β–expansin) proteins obtained from grass pollen. To understand the evolutionary and structural bases for the selectivity of <styled-content style='fixed-case'>EXPB</styled-content> action, we assessed the extension (creep) response of cell walls from diverse monocot families to <styled-content style='fixed-case'>EXPA</styled-content> and <styled-content style='fixed-case'>EXPB</styled-content> treatments. Cell walls from Cyperaceae and Juncaceae (families closely related to grasses) displayed a typical grass response (‘β–response’). Walls from more distant monocots, including some species that share with grasses high levels of arabinoxylan, responded preferentially to α–expansins (‘α–response’), behaving in this regard like eudicots. An expansin with selective activity for grass cell walls was detected in Cyperaceae pollen, coinciding with the expression of genes from the divergent <styled-content style='fixed-case'>EXPB</styled-content> –I branch that includes grass pollen β–expansins. The evolutionary origin of this branch was located within Poales on the basis of phylogenetic analyses and its association with the ‘sigma’ whole‐genome duplication. Accelerated evolution in this branch has remodeled the protein surface in contact with the substrate, potentially for binding highly substituted arabinoxylan. We propose that the evolution of the divergent <styled-content style='fixed-case'>EXPB</styled-content> –I group made a fundamental change in the target and mechanism of wall loosening in the grass lineage possible, involving a new structural role for xylans and the expansins that target them.