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First published online June 8, 2007; 10.1105/tpc.107.051391

The Plant Cell 19:1947-1963 (2007)
© 2007 American Society of Plant Biologists

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Structural Evidence for the Evolution of Xyloglucanase Activity from Xyloglucan Endo-Transglycosylases: Biological Implications for Cell Wall Metabolism[W]

Martin J. Baumanna, Jens M. Eklöfa, Gurvan Michelb, Åsa M. Kallasa, Tuula T. Teeria, Mirjam Czjzekb,1 and Harry Brumer, IIIa,1

a School of Biotechnology, Royal Institute of Technology, AlbaNova University Center, S-10691 Stockholm, Sweden
b Equipe Glycobiologie Marine, Unité Mixte de Recherche 7139, Végétaux Marins et Biomolécules, Centre National de la Recherche Scientifique/Université Pierre et Marie Curie-Paris 6, Station Biologique, 29682 Roscoff, Bretagne, France

1 To whom correspondence should be addressed. E-mail czjzek{at}sb-roscoff.fr or harry{at}biotech.kth.se; fax 33-298-292-324 or 46-8-5537-8367.

High-resolution, three-dimensional structures of the archetypal glycoside hydrolase family 16 (GH16) endo-xyloglucanases Tm-NXG1 and Tm-NXG2 from nasturtium (Tropaeolum majus) have been solved by x-ray crystallography. Key structural features that modulate the relative rates of substrate hydrolysis to transglycosylation in the GH16 xyloglucan-active enzymes were identified by structure–function studies of the recombinantly expressed enzymes in comparison with data for the strict xyloglucan endo-transglycosylase Ptt-XET16-34 from hybrid aspen (Populus tremula x Populus tremuloides). Production of the loop deletion variant Tm-NXG1-{Delta}YNIIG yielded an enzyme that was structurally similar to Ptt-XET16-34 and had a greatly increased transglycosylation:hydrolysis ratio. Comprehensive bioinformatic analyses of XTH gene products, together with detailed kinetic data, strongly suggest that xyloglucanase activity has evolved as a gain of function in an ancestral GH16 XET to meet specific biological requirements during seed germination, fruit ripening, and rapid wall expansion.




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