Adaptações moleculares no desenvolvimento de Parkia platycephala e Stryphnodendron pulcherrimum em substratos de canga e resíduos de mineração

Abstract

Canga is the Brazilian term for savanna-like vegetation harboring several endemic species on iron-rich rocky outcrops and often industrial mining activities. Environmental legislation demands the rehabilitation of degraded areas to minimize environmental impacts. Despite the urgent demand for sustainable mining, the revegetation and rehabilitation of areas degraded by mining activities remain challenging. Parkia platycephala Benth. and Stryphnodendron pulcherrimum (Willd.) Hochr. naturally occur in the cangas of Serra dos Carajás (eastern Amazonia, Brazil) and the surrounding forest, indicating high phenotypic plasticity, and have been studied for the recovery of mining areas. The morphological and physiological mechanisms of the plants’ establishment in the canga environment are well studied, but not the molecular adaptative responses. We constructed complete and accurate transcriptomes from the two Fabaceae species to characterize the gene expression plasticity and understand the adaptive genetic mechanisms behind the establishment in the canga and forest environments. Further, we examined the species growth in mine wastes to evaluate if the shift in the gene expression profile fosters acclimation. The results may reveal relevant molecular mechanisms for land rehabilitation, especially under a changing climate. Plants were grown in substrates of canga, an adjacent forest, and mine residues collected in the Carajás Mineral Province, Pará, Brazil. RNA was extracted from pooled leaf tissue. A combination of methods was utilized to assembly Illumina RNA-seq paired-end reads into two representative transcriptomes forP. platycephala and S. pulcherrimum containing 31,728 and 31,311 primary transcripts, respectively. We identified shared and species-specific molecular responses to the plants’ growth in the substrates using differential expression analysis. In the species-specific analysis on naturally occurring substrates, we identified 1,112 and 838 differentially expressed genes for P. platycephala and S. pulcherrimum, respectively. Enrichment analyses showed unique biological processes and metabolic pathways affected for each species. Comparative differential expression analysis was based on shared single-copy orthologs. The overall pattern of ortholog expression was species-specific. Even so, almost 300 genes were identified differentially expressed between plants in canga and forest substrates, responding the same way in both species. The genes were functionally associated with the response to light stimulus and the circadian rhythm pathway. We also evaluate the performance of the species on degraded area substrates, indicating different performances in the development related to different nutritional needs among them. S. pulcherrimum showed adaptive responses related to phosphorus limitation in substrates. P. platycephala was more successful in the mine waste substrates, showing no changes related to stress conditions. Orthologous circadian rhythm genes were also similarly changed in both species in response to the mine waste substrates. Our results suggest that plants can adjust the circadian rhythm in a substrate-dependent manner. The circadian clock gene modulation might be a central mechanism regulating the plants’ development according to nutrient availability in the studied legume species, shared as a common mechanism to abiotic stress compensation in other native species. This study demonstrates that the plants have common and specific mechanisms that enable their survival in distinct environments such as forest and canga. The results contribute to the enhancement of land rehabilitation practices and the biology of Fabaceae, especially in a climate-changing scenario.