Extremophiles as a Model of a Natural Ecosystem: Transcriptional Coordination of Genes Reveals Distinct Selective Responses of Plants Under Climate Change Scenarios

Abstract

The goal of this research was to generate networks of co-expressed genes to explore the genomic responses of Rhizophora mangle L. populations to contrasting environments and to use gene network analysis to investigate their capacity for adaptation in the face of historical and future perturbations and climatic changes. RNA sequencing data were generated for R. mangle samples collected under field conditions from contrasting climate zones in the equatorial and subtropical regions of Brazil. A gene co-expression network was constructed using Pearson’s correlation coefficient, showing correlations among 78,364 transcriptionally coordinated genes. Each region exhibited two distinct network profiles; genes correlated with the oxidative stress response showed higher relative expression levels in subtropical samples than in equatorial samples, whereas genes correlated with the hyperosmotic salinity response, heat response and UV response had higher expression levels in the equatorial samples than in the subtropical samples. In total, 992 clusters had enriched ontology terms, which suggests that R. mangle is under higher stress in the equatorial region than in the subtropical region. Increased heat may thus pose a substantial risk to species diversity at the center of its distribution range in the Americas. This study, which was performed using trees in natural field conditions, allowed us to associate the specific responses of genes previously described in controlled environments with their responses to the local habitat where the species occurs. The study reveals the effects of contrasting environments on gene expression in R. mangle, shedding light on the different abiotic variables that may contribute to the genetic divergence previously described for the species through the use of simple sequence repeats (SSRs). These effects may result from two fundamental processes in evolution, namely, phenotypic plasticity and natural selection.

Geographical and environmental contributions to genomic divergence in mangrove forests

“…These results corroborate the findings reported by Cruz et al (2020), who performed a functional characterization of putative loci under selection and suggested that differential precipitation regimes play a fundamental role in genetic divergence between populations of this species. Additionally, our findings support the results reported by Bajay et al (2018), who found different profiles of gene expression among populations of Rhizophora mangle located at contrasting latitudes of the Brazilian coast, with differentially expressed genes putatively involved in the responses to variations in temperature, solar radiation, precipitation and flood frequency. The results obtained for both species corroborate the data from other studies reporting that precipitation and air and sea temperature variables are limiting factors regulating the distribution of coastal species (McKee et al, 2012;Soares et al, 2012;Osland et al, 2016;Duke et al, 2017;Cavanaugh et al, 2018;Ximenes et al, 2018).…”

Global Warming, Climate Change, and Environmental Pollution: Recipe for a Multifactorial Stress Combination Disaster

“…A completely different approach could be to focus on pathways and genes that are unique to a multifactorial stress combination [31]. An additional strategy could be to identify and study plants that are subjected to extreme and multifactorial stress conditions in nature (e.g., desert plants, plants growing under harsh conditions in industrial waste sites, salt marshes, and/or next to hot springs, and/or some invasive species) [84][85][86], and…”

Genetic and molecular mechanisms underlying mangrove adaptations to intertidal environments

“…KcTrxf reduces stomatal aperture and promotes stomatal closure to retain water balance in leaves to overcome drought conditions ( Jing et al., 2020 ). Heat shock protein expression induced in response to oxidative stress is also correlated with induction of stomatal closure as acclimatization to heat stress ( Bajay et al., 2018 ). Sooner or later, the stress-driven changes in stomatal opening and closure upset photosynthesis in the leaves.…”

“…In conjunction with stomatal closure, cuticles act as a barrier to water loss and the genes related to cuticle formation are clustered with that of oxidative stress response ( Bajay et al., 2018 ). 3-Ketoacyl-CoA synthase is the key gene involved in cutin, suberin, and wax formation which is highly expressed in K. obovata ( Su et al., 2019 ).…”

“…Overexpression of N. fruticans -specific gene namely hydroxysteroid dehydrogenase ( HSD1 ) in A. thaliana terminated seed dormancy which catalyzes seed lipid biosynthesis and may be responsible for the unusual viviparous seed germination in mangroves ( He et al., 2015 ). Ent kaurene synthase ( KS ) gene and SAE-2 which underwent duplication and amino acid substitution, respectively, in Rhizophoreae mangroves may also be linked to vivipary ( Bajay et al., 2018 ; Xu et al., 2017 ).…”