Demonstration of plants and fungi coevolution

The group of Prof. Angel T. Martínez at Centro de Investigaciones Biológicas has recently published in Proceedings of the National Academy of Sciences the results of a research which demonstrates that the evolution of lignin-degrading enzymes follows lignin evolution in woody plants.

During the last years, many research groups have focused on the evolution of wood-rotting fungi and their enzymatic machinery, due to their ecological and biotechnological relevance. The origin of these important organisms was established in the Carboniferous period, associated to the production of the first ligninolytic peroxidases. Together with other geochemical factors, the rise of wood-rotting fungi ended the coal accumulation signature of this period. Posterior studies on the order Polyporales demonstrated that the ancestor of wood-rotting species was a white-rot fungus (able to mineralize the recalcitrant lignin polymer), while further loss of ligninolytic peroxidases genes generated the brown-rot lineage (which only degrades the sugars of the lignocellulose).

Previous work by the group of Prof. Angel T. Martínez at CIB has resurrected the ancestors of ligninolytic enzymes in Polyporales, where most white-rot fungi are included, demonstrating so far that lignin peroxidases, the most efficient lignin-degrading enzymes, shaped their properties during evolution for a more efficient lignin modification. Their evolution started with a poor lignin oxidation via Mn(III) chelates. Later, they incorporated a solvent exposed tryptophan for direct lignin oxidation, concomitantly with a stabilization to the acidic pH where these fungi act in nature. Together with a progressively more negative charge surrounding the solvent-exposed tryptophan and a generalized boost in their reduction potentials, these peroxidases became the most efficient lignin-degrading enzymes existing today.

In the work now published in PNAS, Ayuso-Fernández et al. have demonstrated using state-of-the-art analytical techniques, such as stopped-flow spectrophotometry and 2D-NMR, that with the incorporation of the solvent-exposed tryptophan there was a dramatic change in the activity and substrate preference of ligninolytic peroxidases. This way, with the appearance of the oxidation site for direct lignin degradation, these enzymes changed their substrate preference from lignin of gymnosperms, more primitive and simpler, to lignin of angiosperms, more recent, complex and recalcitrant due to incorporation of syringyl (S) units to the guaiacyl (G) units forming the gymnosperm lignin. Also, they show that those Polyporales with a higher number of enzymes containing the catalytic tryptophan have a preference to grow on angiosperm wood. Finally, they time-calibrated the phylogeny of Polyporales peroxidases using the fossil record. The rise of the solvent-exposed tryptophan was ~200 mya, concurrent with the appearance and explosive diversification of angiosperms in evolution, pointing with the above results to a fascinating coevolution between saprotrophic fungi and vascular plants.

This work is part of a collaboration of the CIB authors with the CSIC Institute of Natural Resources and Agrobiology of Seville.

Reference: Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants. Ayuso-Fernández I, Rencoret J, Gutiérrez A, Ruiz-Dueñas FJ, Martínez AT [2019]. Proc. Natl. Acad. Sci. DOI: 10.1073/pnas.1905040116

More information: CSIC press release