Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour

Abstract

Background During maturation seeds acquire several physiological traits to enable them to survive drying and disseminate the species. Few studies have addressed the regulatory networks controlling acquisition of these traits at the tissue level particularly in endospermic seeds such as tomato, which matures in a fully hydrated environment and does not undergo maturation drying. Using temporal RNA-seq analyses of the different seed tissues during maturation, gene network and trait-based correlations were used to explore the transcriptome signatures associated with desiccation tolerance, longevity, germination under water stress and dormancy.Results During maturation, 15,173 differentially expressed genes were detected, forming a gene network representing 21 expression modules, with 3 being specific to seed coat and embryo and 5 to the endosperm. A gene-trait significance measure identified a common gene module between endosperm and embryo associated with desiccation tolerance and conserved with non-endospermic seeds. In addition to genes involved in protection such LEA and HSP and ABA response, the module included antioxidant and repair genes. Dormancy was released concomitantly with the increase in longevity throughout fruit ripening until 14 days after the red fruit stage. This was paralleled by an increase in SlDOG1-2 and PROCERA transcripts. The progressive increase in seed vigour was captured by three gene modules, one in common between embryo and endosperm and two tissue-specific. The common module was enriched with genes associated with mRNA processing in chloroplast and mitochondria (including penta- and tetratricopeptide repeat-containing proteins) and post-transcriptional regulation, as well several flowering genes. The embryo-specific module contained homologues of ABI4 and CHOTTO1 as hub genes associated with seed vigour, whereas the endosperm-specific module revealed a diverse set of processes that were related to genome stability, defence against pathogens and ABA/GA response genes. Conclusion The spatio-temporal co-expression atlas of tomato seed maturation will serve as a valuable resource for the in-depth understanding of the dynamics of gene expression associated with the acquisition of seed vigour at the tissue level.

ABSCISIC ACID INSENSITIVE 4 coordinates eoplast formation to ensure acquisition of seed longevity during maturation in Medicago truncatula

“…As inference from gene co‐expression analyses suggested that MtABI4 was linked to longevity (Bizouerne et al., 2021; Verdier et al., 2013), the longevity of the Mtabi4 seeds was determined by monitoring the loss of germination of after‐ripened seeds during storage at 35°C and 75% RH. Seed lifespan was reduced by 75% in Mtabi4 compared with the WT (Figure 2a).…”

“…Gene co‐expression analyses during maturation in seeds of Medicago truncatula and Solanum lycopersicum (tomato) identified ABI4 as a transcription factor correlated with seed longevity (Bizouerne et al., 2021; Verdier et al., 2013). ABI4 is a versatile enhancer of ABA signal transduction during development and in response to stress.…”

Chromatin dynamics associated with seed desiccation tolerance/sensitivity at early germination in Medicago truncatula

“…The molecular processes involved in DT acquisition and reinduction have been well studied at the transcriptomic level, which resulted in identification of DT-associated gene networks. These DT-associated genes were mainly associated with cell protection functions (e.g., antioxidants and protective compounds), promoting cell survival upon severe dehydration (Delahaie et al, 2013;Terrasson et al, 2013;Verdier et al, 2013;Costa et al, 2015;Righetti et al, 2015;Gonzaĺez-Morales et al, 2016;Costa et al, 2017;Bizouerne et al, 2021). These DTassociated gene networks are transcriptionally regulated at potentially two levels: a more explored direct transcriptional regulation via the action of transcriptional activators/repressors such as transcription factors and/or at the epigenetic level via the regulation of the chromatin accessibility rendering the DTassociated genes in a repressed or activable states.…”

Network Biology Analyses and Dynamic Modeling of Gene Regulatory Networks Under Drought Stress Reveal Major Transcriptional Regulators in Arabidopsis

“…Henceforth, topological features of a system and network architectural analyses can be employed to identify novel molecular players and regulators in various regulatory networks in diverse systems [14,[26][27][28][29]. Among these network features, modules (clusters of highly correlated genes) and hubs (high degree; the number of edges of a node) have been used to predict major regulators in Arabidopsis and tomato [14,30]. Modeling dynamic transcriptional processes in TRNs is challenging, but it can hold a great promise to comprehend how plants respond to water scarcity.…”