Major Domestication-Related Phenotypes in Indica Rice Are Due to Loss of miRNA-Mediated Laccase Silencing.

Chenna Swetha,Debjani Basu,Ashwin Nair,Varsha Tirumalai,P V Shivaprasad,Kannan Pachamuthu,Melvin Prasad

doi:10.1105/tpc.18.00472

Abstract

Domestication of rice (Oryza sativa) included conversion of perennial wild species with few seeds to short plants that produced abundant seeds. Most domestication-associated changes were due to variations in transcription factors and other key proteins such as enzymes. Here, we show that multiple yield-related traits associated with indica rice domestication are linked to micro (mi) RNA-mediated regulation. Analysis of small (s) RNA data sets from cultivated indica rice lines, a few landraces, and two wild relatives of rice revealed the presence of abundant 22-nucleotide (nt) reads in wild relatives that mapped to miR397 precursors. miR397 was expressed at very high levels in wild relatives and at negligible levels in high-yielding cultivated lines. In its genera-specific form of 22-nt, miR397 targeted mRNAs encoding laccases that decayed and induced robust secondary cascade silencing in wild species that required RNA-dependent RNA polymerase 6. In wild species of rice, reduced expression of laccases resulted in low lignification. As expected, overexpression of miR397 induced de-domestication phenotypes. At least 26 uncharacterized QTLs previously implicated in rice yield overlapped with laccases and miR397 genes. These results suggest that miRNAs contribute to rice domestication-associated phenotypes.

Highlights

Indica rice was domesticated from Oryza nivara and O. rufipogon in South and East Asia (Sweeney and McCouch, 2007; Wing et al, 2018)
To explore if domestication-related traits are associated with small RNA-mediated regulation, we initially performed phenotypic analysis of 290 indica rice landraces grown in the Indian sub-continent along with two wild species of rice that are naturally grown (O. nivara and O. rufipogon) and 12 high-yielding cultivated rice lines that are the results of modern breeding
Among the 22-nt reads, there was a strong bias for 5′ U in data sets derived from wild species of rice (Figure 1B and Supplemental Figure 1E), indicating that the majority of these 22-nt small regulatory RNAs (sRNAs) were likely associated with AGO1 or its close homologs

Summary

INTRODUCTION

GIF1, and Rc, have been cloned and functionally characterized (Kovach et al, 2007; Izawa, 2008) In such instances, simple changes in the promoter sequences of these genes altered their expression (Huo et al, 2017), while in some cases insertion of a transposon was responsible (Li et al, 2017). It is well established that phenotypic diversity of domesticated crops is not proportional to genomic changes (Meyer and Purugganan, 2013). It has been found that heritable phenotypes of hybrids are likely due to epigenetics and small regulatory RNAs (sRNAs) (Shivaprasad et al, 2012b; Bond and Baulcombe, 2014). Several epialleles have strong genetic linkage to changes in phenotypes of crops and the DNA methylation status in the regulatory sequences of the genes (Manning et al, 2006; Niederhuth and Schmitz, 2014)

RESULTS

DISCUSSION

METHODS