A MYB4-MAN3-Mannose-MNB1 signaling cascade regulates cadmium tolerance in Arabidopsis.

Xingxing Yan,Qingliu Geng,Cheng Zhang,Feng Chen,Tingting Fan,Xi Wu,Ying Huang,Hui Song,Shuqing Cao,Min Hu,Gregory P Copenhaver

doi:10.1371/journal.pgen.1009636

Abstract

Our previous studies showed that MAN3-mediated mannose plays an important role in plant responses to cadmium (Cd) stress. However, the underlying mechanisms and signaling pathways involved are poorly understood. In this study, we showed that an Arabidopsis MYB4-MAN3-Mannose-MNB1 signaling cascade is involved in the regulation of plant Cd tolerance. Loss-of-function of MNB1 (mannose-binding-lectin 1) led to decreased Cd accumulation and tolerance, whereas overexpression of MNB1 significantly enhanced Cd accumulation and tolerance. Consistently, expression of the genes involved in the GSH-dependent phytochelatin (PC) synthesis pathway (such as GSH1, GSH2, PCS1, and PCS2) was significantly reduced in the mnb1 mutants but markedly increased in the MNB1-OE lines in the absence or presence of Cd stress, which was positively correlated with Cd-activated PC synthesis. Moreover, we found that mannose is able to bind to the GNA-related domain of MNB1, and that mannose binding to the GNA-related domain of MNB1 is required for MAN3-mediated Cd tolerance in Arabidopsis. Further analysis showed that MYB4 directly binds to the promoter of MAN3 to positively regulate the transcript of MAN3 and thus Cd tolerance via the GSH-dependent PC synthesis pathway. Consistent with these findings, overexpression of MAN3 rescued the Cd-sensitive phenotype of the myb4 mutant but not the mnb1 mutant, whereas overexpression of MNB1 rescued the Cd-sensitive phenotype of the myb4 mutant. Taken together, our results provide compelling evidence that a MYB4-MAN3-Mannose-MNB1 signaling cascade regulates cadmium tolerance in Arabidopsis through the GSH-dependent PC synthesis pathway.

Highlights

The heavy metal cadmium (Cd) is a toxic trace pollutant for humans, animals and plants, which enters the environment mainly from the burning of fossil fuels and phosphate fertilizers and the food chain [1,2,3]
Our results demonstrated that a MYB4-MAN3-Mannose-MNB1 signaling cascade regulates Cd tolerance through the GSH-dependent PC synthesis pathway in Arabidopsis
It was shown that MAN3-mediated mannose is involved in the regulation of Cd stress response in Arabidopsis [37], and the pepper mannose-binding lectin CaMBL1 has been shown to be involved in defense against microbial pathogens [32]

Summary

Introduction

The heavy metal cadmium (Cd) is a toxic trace pollutant for humans, animals and plants, which enters the environment mainly from the burning of fossil fuels and phosphate fertilizers and the food chain [1,2,3]. A number of key genes have been shown to be involved in regulation of Cd detoxification and tolerance in different plant species, such as ZNT1, GSH1, OsHMA9, AtPDR8, ZntA, CAD2, ATM3, Nramp, and ACBP1 [4,7,12,13,14,15,16,17,18,19,20]. Recent studies demonstrate that transcription factors are critical components in regulating Cd detoxification and tolerance in plants, such as HsfA4a [23], bHLH29, bHLH38, and bHLH39 [24], ZAT6 [25], OXIDATIVE STRESS2 [26], and MYB49 [27]. Whether and how MYB4 regulates the plant response to Cd stress remains unknown

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Conclusion