The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism.

Qingzhu Zhang,Dong Wang,Cheng Zhao,Zhizhong Gong,Juan Dong,Dong-Lei Yang,Ashish Kumar Srivastava,Li He,Tao Xu,Lan Yang,Heng Zhang,Renyi Liu,Liang Zeng,Yanqiang Li,Jian-Kang Zhu,Zhimin Zheng

doi:10.1038/celldisc.2016.27

Abstract

In plants, hybrid vigor is influenced by genetic and epigenetic mechanisms; however, the molecular pathways are poorly understood. We investigated the potential contributions of epigenetic regulators to heterosis in Arabidposis and found that the chromatin remodeler DECREASED DNA METHYLATION 1 (DDM1) affects early seedling growth heterosis in Col/C24 hybrids. ddm1 mutants showed impaired heterosis and increased expression of non-additively expressed genes related to salicylic acid metabolism. Interestingly, our data suggest that salicylic acid is a hormetic regulator of seedling growth heterosis, and that hybrid vigor arises from crosses that produce optimal salicylic acid levels. Although DNA methylation failed to correlate with differential non-additively expressed gene expression, we uncovered DDM1 as an epigenetic link between salicylic acid metabolism and heterosis, and propose that the endogenous salicylic acid levels of parental plants can be used to predict the heterotic outcome. Salicylic acid protects plants from pathogens and abiotic stress. Thus, our findings suggest that stress-induced hormesis, which has been associated with increased longevity in other organisms, may underlie specific hybrid vigor traits.

Highlights

Hybrid vigor, or heterosis, refers to the improved performance of hybrid offspring relative to their parents
We found that F1 seedlings from wild type (WT), rdr2, dms3, drd1, rdm1, nrpd1, nrpe1, ago4, ago6 and rdm3 crosses displayed a significant increase in leaf width compared with their respective parents, indicating a heterosis phenotype (Figure 1)
The tested RNA-directed DNA methylation (RdDM) mutants maintained heterosis, at least during the early seedling stage. These results are consistent with recent work in Arabidopsis [14] and with the observation in maize that loss of MOP1, an RNA-dependent RNA polymerase 2 (RDR2) ortholog in the RdDM pathway in maize, did not affect the hybrid vigor of B73 × Mo17 hybrids [15]

Summary

Introduction

Heterosis, refers to the improved performance of hybrid offspring relative to their parents. In the current model of RdDM, de novo DNA methylation is initiated by the production of 24-nt small interfering RNAs (siRNAs), which are generated by a set of factors, including a plant-specific RNA polymerase (Pol IV), RNA-dependent RNA polymerase 2 (RDR2) and Dicer-like 3. These 24-nt siRNAs are loaded onto AGO4/6 to form an AGO4/6–siRNA complex. DOMAINS REARRANGED METHYLTRANSFERASE 2 is recruited to this complex and mediates de novo methylation of cytosines in all sequence contexts (CG, CHG and CHH, where H represents A, C or T) This results in transcriptional silencing at genomic loci transcribed by Pol V. RdDM has been found to occur at a wide range of genomic locations but with preferences for euchromatic regions

Methods

Results

Conclusion