HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants

<jats:title>Abstract</jats:title><jats:p>Melatonin regulates broad aspects of plant responses to various biotic and abiotic stresses, but the upstream regulation of melatonin biosynthesis by these stresses remains largely unknown. Herein, we demonstrate that transcription factor heat‐shock factor A1a (HsfA1a) conferred cadmium (Cd) tolerance to tomato plants, in part through its positive role in inducing melatonin biosynthesis under Cd stress. Analysis of leaf phenotype, chlorophyll content, and photosynthetic efficiency revealed that silencing of the <jats:italic>HsfA1a</jats:italic> gene decreased Cd tolerance, whereas its overexpression enhanced plant tolerance to Cd. <jats:italic>HsfA1a</jats:italic>‐silenced plants exhibited reduced melatonin levels, and <jats:italic>HsfA1a</jats:italic> overexpression stimulated melatonin accumulation and the expression of the melatonin biosynthetic gene caffeic acid <jats:italic>O</jats:italic>‐methyltransferase 1 (<jats:italic><jats:styled-content style="fixed-case">COMT</jats:styled-content>1</jats:italic>) under Cd stress. Both an in vitro electrophoretic mobility shift assay and in vivo chromatin immunoprecipitation coupled with <jats:styled-content style="fixed-case">qPCR</jats:styled-content> analysis revealed that HsfA1a binds to the <jats:italic><jats:styled-content style="fixed-case">COMT</jats:styled-content>1</jats:italic> gene promoter. Meanwhile, Cd stress induced the expression of heat‐shock proteins (<jats:italic><jats:styled-content style="fixed-case">HSP</jats:styled-content>s</jats:italic>), which was compromised in <jats:italic>HsfA1a</jats:italic>‐silenced plants and more robustly induced in <jats:italic>HsfA1a</jats:italic>‐overexpressing plants under Cd stress. <jats:italic><jats:styled-content style="fixed-case">COMT</jats:styled-content>1</jats:italic> silencing reduced <jats:italic>HsfA1a</jats:italic>‐induced Cd tolerance and melatonin accumulation in <jats:italic>HsfA1a</jats:italic>‐overexpressing plants. Additionally, the <jats:italic>HsfA1a</jats:italic>‐induced expression of <jats:italic><jats:styled-content style="fixed-case">HSP</jats:styled-content>s</jats:italic> was partially compromised in <jats:italic><jats:styled-content style="fixed-case">COMT</jats:styled-content>1</jats:italic>‐silenced wild‐type or <jats:italic>HsfA1a</jats:italic>‐overexpressing plants under Cd stress. These results demonstrate that HsfA1a confers Cd tolerance by activating transcription of the <jats:italic><jats:styled-content style="fixed-case">COMT</jats:styled-content>1</jats:italic> gene and inducing accumulation of melatonin that partially upregulates expression <jats:italic>of <jats:styled-content style="fixed-case">HSP</jats:styled-content>s</jats:italic>.</jats:p>