Evolution of chlorophyll degradation is associated with plant transition to land

Abstract

Colonization of land by green plants (Viridiplantae) some 500 million years ago was made possible by large metabolic and biochemical adaptations. Chlorophyll, the central pigment of photosynthesis, is highly photoactive. In order to mitigate deleterious effects of pigment accumulation, some plants have evolved a coordinated pathway to deal with chlorophyll degradation end-products, so-called phyllobilins. This pathway has been so far mostly unravelled in Arabidopsis thaliana. Here, large-scale comparative phylogenomic coupled to an innovative biochemical characterization strategy of phyllobilins allow a better understanding of how such a pathway appeared in Viridiplantae. Our analysis reveals a stepwise evolution of the canonical pheophorbide a monooxygenase/phyllobilin pathway. It appears to have evolved gradually, first in chlorophyte's chloroplasts, to ensure multicellularity by detoxifying chlorophyll catabolites, and in charophytes outside chloroplasts to allow adaptation of embryophytes to land. At least six out of the eight genes involved in the pathway were already present in the last common ancestor of green plants. This strongly suggests parallel evolution of distinct enzymes catalysing similar reactions in various lineages, particularly for the dephytylation step. Together, our study suggests that chlorophyll detoxification accompanied the transition from water to land, and was therefore of great importance for plant diversification.

Chlorophyll dephytylase 1 and chlorophyll synthase: a chlorophyll salvage pathway for the turnover of photosystems I and II

“…Further analysis is required to clarify these controversial issues. Finally, CLD homologs have been found in cyanobacterial genomes (Schumacher et al., 2022), but no CLH genes. Therefore, it is more likely that these CLD isoforms have evolved for Chl salvage during the turnover of the two photosystems, as cyanobacteria use a D1 repair cycle similar to that of plants.…”

Side‐chain modifications of phyllobilins may not be essential for chlorophyll degradation in Arabidopsis

“…Although these three side-chain modifications have been described, the structural diversity of phyllobilins observed (Schumacher et al, 2021) suggests a much larger range of unknown reactions are associated with phyllobilins processing. Some other examples of side-chain modification have been described, like F I G U R E 1 Chlorophyll (left) is degraded through the PAO/phyllobilin pathway and produces a diverse range of linear tetrapyrroles: the phyllobilins (right).…”

“…Although these three side‐chain modifications have been described, the structural diversity of phyllobilins observed (Schumacher et al, 2021) suggests a much larger range of unknown reactions are associated with phyllobilins processing. Some other examples of side‐chain modification have been described, like hypermodified FCCs (hmFCCs) detected, for example, in ripe banana ( Musa sp.)…”

“…hmFCCs are stabilized due to functionalization of the C12 propionic acid with different groups (Oberhuber et al, 2008). Some gymnosperms and ferns like Pteridium aquilinum accumulate iso‐phyllobilanones, which present a major carbon‐skeleton rearrangement (Erhart et al, 2018; Schumacher et al, 2021). Given some phyllobilins are also bioactive compounds with antioxidative and anti‐inflammatory compounds (Wang et al, 2021), understanding the molecular basis of their synthesis and accumulation could bring interesting insight outside plant sciences toward potential pharmacological applications.…”

“…To date, at least nine distinct FCC-derived structures have been described in Arabidopsis that are modified on their peripheral side chains at five distinct positions on the molecule (C1, C2, C4, C3 2 , and C8 4 , respectively; Figure 1). A recent survey of over 183 species revealed a much larger diversity, with potentially more than 40 distinct phyllobilin structures to be found in green plants (Schumacher et al, 2021). All these phyllobilins are classified based on their structure into two categories: Type I, nonfluorescent (NCCs), 1-formyl and 19-oxobilins, and Type II, dioxobilin-type (DNCCs) (Kräutler, 2014(Kräutler, , 2016.…”