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Physiological and transcriptomic analyses reveal the roles of secondary metabolism in the adaptive responses of Stylosanthes to manganese toxicity.

ABSTRACT: Background: As a heavy metal, manganese (Mn) can be toxic to plants. Stylo (Stylosanthes) is an important tropical legume that exhibits tolerance to high levels of Mn. However, little is known about the adaptive responses of stylo to Mn toxicity. Thus, this study integrated both physiological and transcriptomic analyses of stylo subjected to Mn toxicity.

Results: Results showed that excess Mn treatments increased malondialdehyde (MDA) levels in leaves of stylo, resulting in the reduction of leaf chlorophyll concentrations and plant dry weight. In contrast, the activities of enzymes, such as peroxidase (POD), phenylalanine ammonia-lyase (PAL) and polyphenol oxidase (PPO), were significantly increased in stylo leaves upon treatment with increasing Mn levels, particularly Mn levels greater than 400??M. Transcriptome analysis revealed 2471 up-regulated and 1623 down-regulated genes in stylo leaves subjected to Mn toxicity. Among them, a set of excess Mn up-regulated genes, such as genes encoding PAL, cinnamyl-alcohol dehydrogenases (CADs), chalcone isomerase (CHI), chalcone synthase (CHS) and flavonol synthase (FLS), were enriched in secondary metabolic processes based on gene ontology (GO) analysis. Numerous genes associated with transcription factors (TFs), such as genes belonging to the C2H2 zinc finger transcription factor, WRKY and MYB families, were also regulated by Mn in stylo leaves. Furthermore, the C2H2 and MYB transcription factors were predicted to be involved in the transcriptional regulation of genes that participate in secondary metabolism in stylo during Mn exposure. Interestingly, the activation of secondary metabolism-related genes probably resulted in increased levels of secondary metabolites, including total phenols, flavonoids, tannins and anthocyanidins.

Conclusions: Taken together, this study reveals the roles of secondary metabolism in the adaptive responses of stylo to Mn toxicity, which is probably regulated by specific transcription factors.

SUBMITTER: Jia Y

PROVIDER: S-EPMC7713027 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Physiological and transcriptomic analyses reveal the roles of secondary metabolism in the adaptive responses of Stylosanthes to manganese toxicity.

Jia Yidan Y Li Xinyong X Liu Qin Q Hu Xuan X Li Jifu J Dong Rongshu R Liu Pandao P Liu Guodao G Luo Lijuan L Chen Zhijian Z

BMC genomics 20201203 1

<h4>Background</h4>As a heavy metal, manganese (Mn) can be toxic to plants. Stylo (Stylosanthes) is an important tropical legume that exhibits tolerance to high levels of Mn. However, little is known about the adaptive responses of stylo to Mn toxicity. Thus, this study integrated both physiological and transcriptomic analyses of stylo subjected to Mn toxicity.<h4>Results</h4>Results showed that excess Mn treatments increased malondialdehyde (MDA) levels in leaves of stylo, resulting in the redu ...[more]

PMID: 33272205

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Project description:BackgroundManganese (Mn), an essential element for plants, can be toxic when present in excess. Stylo (Stylosanthes) is a pioneer tropical legume with great potential for Mn tolerance, but its Mn tolerance mechanisms remain poorly understood.ResultsIn this study, variations in Mn tolerance were observed among nine stylo genotypes. Stylo genotype 'RY5' exhibited the highest Mn tolerance compared to the other tested genotypes, whereas 'TF2001' was a Mn-sensitive genotype. The mechanisms underlying the response of stylo to Mn toxicity were further investigated using these two genotypes with contrasting Mn tolerance. Results showed that stylo genotype RY5 exhibited Mn tolerance superior to that of genotype TF2001, showing lower reductions in leaf chlorophyll concentration, chlorophyll fluorescence parameters, photosynthetic indexes and plant dry weight under Mn toxicity. A label-free quantitative proteomic analysis was conducted to investigate the protein profiles in the leaves and roots of RY5 in response to Mn toxicity. A total of 356 differentially expressed proteins (DEPs) were identified, including 206 proteins from leaves and 150 proteins from roots, which consisted of 71 upregulated, 62 downregulated, 127 strongly induced and 96 completely suppressed proteins. These DEPs were mainly involved in defense response, photosynthesis, carbon fixation, metabolism, cell wall modulation and signaling. The qRT-PCR analysis verified that 10 out of 12 corresponding gene transcription patterns correlated with their encoding proteins after Mn exposure. Finally, a schematic was constructed to reveal insights into the molecular processes in the leaves and roots of stylo in response to Mn toxicity.ConclusionsThese findings suggest that stylo plants may cope with Mn toxicity by enhancing their defense response and phenylpropanoid pathways, adjusting photosynthesis and metabolic processes, and modulating protein synthesis and turnover. This study provides a platform for the future study of Mn tolerance mechanisms in stylo and may lead to a better understanding of the potential mechanisms underlying tropical legume adaptation to Mn toxicity.

Project description:BACKGROUND:Citrus blight is a very important progressive decline disease of commercial citrus. The etiology is unknown, although the disease can be transmitted by root grafts, suggesting a viral etiology. Diagnosis is made by demonstrating physical blockage of xylem cells that prevents the movement of water. This test was used to identify symptomatic trees from four commercial groves in Florida. Total RNA extracts of phloem-enriched scaffold root tissues were prepared from seven trees that failed to take up water and from one healthy tree. These RNA extracts were used for transcriptomic analyses using paired end RNA-Seq from an Illumina 2500 system. The expression of transcripts annotated as polyprotein of citrus endogenous pararetrovirus were estimated by both RT-qPCR and RNA-Seq. RESULTS:Transcripts from seven RNA-Seq libraries from trees affected by citrus blight were compared to a control tree. 129-148 million RNA fragments (two paired-end reads/fragment) were generated per library and were mapped to the sweet orange reference genome. In response to citrus blight stress, genes encoding aquaporins, proteins with water channel activity and several cellulose synthase genes were down-regulated, whereas genes involved in lignin and glucosinolate biosynthesis were up-regulated. Transcripts encoding proteins in pathways of carbohydrate metabolism, nucleotide synthesis, signaling, hormone metabolism, secondary metabolism, transport, and biotic stress pathways were overwhelmingly down regulated in all libraries. CONCLUSION:Reduced water intake and xylem plugging were observed in the trees tested and the changes in their transcriptome were analyzed. Plants adapted to reduced water flow by regulating primary and secondary metabolism, nuclear transport and hormone associated pathways. The patterns of energy generation, transcription, translation and protein degradation were consistent with irreversible decline. The down regulation of cellulose synthase transcripts and up regulation of transcripts related to lignin production likely lead to an imbalance in the pathways leading to wood formation, and may lead to the blockage of the xylem vessels seen as the cardinal symptom of citrus blight. Transcripts of a pararetrovirus were elevated in the transcriptome of roots used in this study.

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Physiological and transcriptomic analyses reveal the roles of secondary metabolism in the adaptive responses of Stylosanthes to manganese toxicity.

Publications

Physiological and transcriptomic analyses reveal the roles of secondary metabolism in the adaptive responses of Stylosanthes to manganese toxicity.

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