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

Yidan Jia,Jifu Li,Zhijian Chen,Qin Liu,Guodao Liu,Rongshu Dong,Lijuan Luo,Xuan Hu,Xinyong Li,Pandao Liu

doi:10.1186/s12864-020-07279-2

Abstract

BackgroundAs 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.ResultsResults 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 μM. 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.ConclusionsTaken 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.

Highlights

As a heavy metal, manganese (Mn) can be toxic to plants
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
O2− accumulation was mainly observed in leaves treated with excess Mn compared with the control (5 μM), and the most intense blue color was observed in leaves treated with 800 μM Mn (Fig. 1b)

Summary

Introduction

Manganese (Mn) can be toxic to plants. Stylo (Stylosanthes) is an important tropical legume that exhibits tolerance to high levels of Mn. Excess Mn toxicity generally occurs in acid soils due to the accumulation of bioactive divalent Mn (II) [5, 6] Soil amelioration, such as lime application, is typically conducted to alleviate Mn toxicity by decreasing Mn availability, but this application is costly from both economic and environmental aspects [7]. For these reasons, breeding crop varieties with superior Mn tolerance represents a sustainable alternative agronomical strategy, but this strategy requires better understanding of how plants respond to Mn toxicity. Adverse impacts caused by Mn toxicity have been documented in plant cells at physiological levels, such as triggering oxidative stress, causing lipid peroxidation, inhibiting enzyme activity, impairing chlorophyll biosynthesis and photosynthesis and disturbing the uptake and translocation of other mineral elements [1, 9]

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Conclusion