Seed mucilage evolution: diverse molecular mechanisms generate versatile ecological functions for particular environments

Abstract

Polysaccharidic mucilage is a widespread plant trait with diverse features, often present around plant structures in contact with the environment, providing numerous functions including protection and adhesion. Seed mucilage is released upon imbibition and therefore can play roles in the early seedling stages, but the evolutionary origins of this trait are unclear. Its presence in several flowering plant species suggests that it was present in their last common ancestor whereas the extreme inter-species morphological and chemical natural diversity suggests multiple origins. Here, we summarize the recent advances on molecular mechanisms and ecological functions underlying this inter-and intra-species natural diversity. A master regulatory complex balancing carbon partitioning in seed appears to be conserved among flowering plants with a sequential evolution of its molecular components. At the intra-species level, a high polymorphism was detected for a few genes in relation to the observed morphological diversity. Historically, the ecological functions of seed mucilage were mostly related to germination and seed dissemination but recently some exosystemic functions were uncovered such as soil microorganism control and plant establishment support. These recent advances enable drawing a clearer picture of the seed mucilage evolution, the underlying molecular mechanisms, and the associated ecological roles.

A tale of two morphs: developmental patterns and mechanisms of seed coat differentiation in the dimorphic diaspore model Aethionema arabicum (Brassicaceae)

“…The Ae. arabicum RNA‐seq demonstrated that in contrast to AearNARS1/2 and AearAP2 , TFs of the MYB‐bHLH‐WD40 (MWB) complex (Golz et al , 2018; Viudes et al , 2020; Voiniciuc et al , 2015) did not show a morph‐specific expression difference in flower samples (Figure 6a). Analysis of AearAP2 and AearNARS2 gene expression by RT‐qPCR at 1, 3 and 10 DAP (Figure 6b) not only confirmed that the transcript abundances differ at the flower stage (1 DAP), but also during all the subsequent early stages of seed coat differentiation, particularly at 3 DAP.…”

“…The default monomorphic ‘bauplan’ within the Brassicaceae is the development of dehiscent fruits (DEH) containing mucilaginous seeds (M + ) with A. thaliana and Lepidium sativum as examples (Ferrandiz et al , 1999; Mühlhausen et al , 2013; Scheler et al , 2015). The DEH/M + fruit/seed programme leads to fruit valve opening to release mature M + seeds as diaspores, which upon imbibition release mucilage from their outer seed coats (myxospermy) (Viudes et al , 2020; Western, 2012; Yang et al , 2012). Mutations in A. thaliana fruit development genes, such as the bHLH (basic helix–loop–helix) transcription factor (TF) INDEHISCENT and the MADS‐box TFs SHATTERPROOF1/2 ( SHP1/2 ), block fruit valve opening which phenotypically result in indehiscent fruits (IND) (Mühlhausen et al , 2013).…”

Evolution of environmental stress responses in plants

“…In this Special Issue, three groups of scientists present systematic reviews of their understanding of the evolution of plant salinity tolerance at ecological, physiological, cellular and molecular levels (Caperta et al, 2020;Kotula, Garcia Caparros, Zorb, Colmer, & Flowers, 2020;Liu et al, 2020). Secretory structures (e.g., mucilage secretion, salt glands) are found in all angiosperm clades, with the potential to influence plant microenvironments, nutrient balance and stress tolerance (Galloway, Knox, & Krause, 2020;Viudes et al, 2020). Caperta and co-authors studied the link between secretory structures and salt tolerance in plants using the Plumbaginaceae family, which is adapted to a wide range of arid and saline habitats with at least 45 salt-tolerant species.…”

“…The review by Viudes and colleagues aimed at the under-studied field of myxodiaspory evolution, indicating the release of a polysaccharidic mucilage upon water imbibition of seeds (myxospermy) or fruits (myxocarpy) of myxodiasporous species may have potential roles in plant response to environmental stresses (Viudes, Burlat, & Dunand, 2020). A deep characterization of the molecular actors revealed the mucilage secretory cell (MSC) toolbox that underpins seed mucilage establishment in Arabidopsis thaliana (Francoz, Ranocha, Burlat, & Dunand, 2015).…”

“…A deep characterization of the molecular actors revealed the mucilage secretory cell (MSC) toolbox that underpins seed mucilage establishment in Arabidopsis thaliana (Francoz, Ranocha, Burlat, & Dunand, 2015). Recent studies reported that 94 genes (a majority of them transcription factors) of the MSC toolbox participate in seed mucilage production and release in A. thaliana (Francoz et al, 2015;Viudes et al, 2020). The authors showed that key genes F I G U R E 1 A combination of approaches can be used to address the question how plants have adapted to environmental stress over the course of evolution.…”