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Water-related innovations in land plants evolved by different patterns of gene cooption and novelty.

ABSTRACT: The origin of land plants and their descendants was marked by the evolution of key adaptations to life in terrestrial environments such as roots, vascular tissue and stomata. Though these innovations are well characterized, the evolution of the genetic toolkit underlying their development and function is poorly understood. We analysed molecular data from 532 species to investigate the evolutionary origin and diversification of genes involved in the development and regulation of these adaptations. We show that novel genes in the first land plants led to the single origin of stomata, but the stomatal closure of seed plants resulted from later gene expansions. By contrast, the major mechanism leading to the origin of vascular tissue was cooption of genes that emerged in the first land plants, enabling continuous water transport throughout the ancestral vascular plant. In turn, new key genes in the ancestors of plants with true leaves and seed plants led to the emergence of roots and lateral roots. The analysis highlights the different modes of evolution that enabled plants to conquer land, suggesting that gene expansion and cooption are the most common mechanisms of biological innovation in plant evolutionary history.

SUBMITTER: Bowles AMC

PROVIDER: S-EPMC9303528 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Leaf water conservation and pseudobulb water storage are two of the strategies commonly employed by epiphytic plants to adapt to dry environments. During the flowering period, a great deal of water transpires through the flowers, which then influences water-related processes. However, there is little research on the coordinated relationship between the different structures of epiphytes. Our study explored the phylogenetic conservation and evolutionary correlations between structural traits of 8 species in the genus Dendrobium by using phylogenetic independent contrast (PIC) analysis. RESULTS:Leaf dry mass, leaf water content, leaf dry matter content, specific leaf area, stomatal density, stomatal area index, pseudobulb length, pseudobulb width, and flower dry mass show strong phylogenetic signals. Pseudobulb length is significantly positively correlated with stomatal volume but significantly negatively correlated with mesophyll thickness according to both species mean values and PIC values. Pseudobulb internode length is also positively correlated with stomatal volume but negatively correlated with stomatal density according to PIC values. Pseudobulb width is significantly positively correlated with leaf dry mass, stomatal density, stomatal area index, flower petal vein number and flower dry mass but negatively correlated with specific leaf area according to species mean values. However, these correlations are insignificant when PIC values are analyzed. Stomatal volume is positively correlated with flower dry mass, and after phylogeny is considered, this correlation is still significant. Leaf dry mass is positively correlated with flower petal vein number according to species values. Flower number per pseudobulb is negatively correlated with upper epidermal cell size according to species values but negatively correlated with stomatal area index according to PIC values. There are no correlations between pseudobulb and flower water-related traits according to PIC values. CONCLUSIONS:A trade-off should exist in epiphytic plants between the two drought-tolerant strategies of pseudobulb storage and leaf water retention. Plants possessing thick blades with a few large stomata tend to use the pseudobulb water storage strategy to adapt to drought. Small flowers and low flower dry mass should be associated with the leaf water retention strategy. In addition, flowers and leaves exhibit an obvious water balance and should share common selection pressures. The present study provides a case with which to understand the coordinated adaptation of different structures in epiphytic plants.

Project description:Cytochrome P450 (CYP) monooxygenases and glutathione S-transferases (GST) are enzymes that catalyse chemical modifications of a range of organic compounds. Herbicide resistance has been associated with higher levels of CYP and GST gene expression in some herbicide-resistant weed populations compared to sensitive populations of the same species. By comparing the protein sequences of 9 representative species of the Archaeplastida-the lineage which includes red algae, glaucophyte algae, chlorophyte algae, and streptophytes-and generating phylogenetic trees, we identified the CYP and GST proteins that existed in the common ancestor of the Archaeplastida. All CYP clans and all but one land plant GST classes present in land plants evolved before the divergence of streptophyte algae and land plants from their last common ancestor. We also demonstrate that there are more genes encoding CYP and GST proteins in land plants than in algae. The larger numbers of genes among land plants largely results from gene duplications in CYP clans 71, 72, and 85 and in the GST phi and tau classes [1,2]. Enzymes that either metabolise herbicides or confer herbicide resistance belong to CYP clans 71 and 72 and the GST phi and tau classes. Most CYP proteins that have been shown to confer herbicide resistance are members of the CYP81 family from clan 71. These results demonstrate that the clan and class diversity in extant plant CYP and GST proteins had evolved before the divergence of land plants and streptophyte algae from a last common ancestor estimated to be between 515 and 474 million years ago. Then, early in embryophyte evolution during the Palaeozoic, gene duplication in four of the twelve CYP clans, and in two of the fourteen GST classes, led to the large numbers of CYP and GST proteins found in extant land plants. It is among the genes of CYP clans 71 and 72 and GST classes phi and tau that alleles conferring herbicide resistance evolved in the last fifty years.

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Water-related innovations in land plants evolved by different patterns of gene cooption and novelty.

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