The behavior of transcriptomes and epigenomes in hybrids of heterotic parents is of fundamental interest. Here, we report highly integrated maps of the epigenome, mRNA, and small RNA transcriptomes of two rice (Oryza sativa) subspecies and their reciprocal hybrids. We found that gene activity was correlated with DNA methylation and both active and repressive histone modifications in transcribed regions. Differential epigenetic modifications correlated with changes in transcript levels among hybrids and parental lines. Distinct patterns in gene expression and epigenetic modifications in reciprocal hybrids were observed. Through analyses of single nucleotide polymorphisms from our sequence data, we observed a high correlation of allelic bias of epigenetic modifications or gene expression in reciprocal hybrids with their differences in the parental lines. The abundance of distinct small RNA size classes differed between the parents, and more small RNAs were downregulated than upregulated in the reciprocal hybrids. Together, our data reveal a comprehensive overview of transcriptional and epigenetic trends in heterotic rice crosses and provide a useful resource for the rice community.

Although abscisic acid (ABA) is an important hormone that regulates seed dormancy, stomatal closure, plant development, as well as responses to environmental stimuli, the physiological mechanisms of ABA response to multiple stress in rice remain poorly understood. In the ABA biosynthetic pathway, 9-cis-epoxycarotenoid dioxygenase (NCED) is the key rate-limiting enzyme. Here, we report important functions of OsNCED3 in multi-abiotic stress tolerance in rice. The OsNCED3 is constitutively expressed in various tissues under normal condition, Its expression is highly induced by NaCl, PEG, and H2O2 stress, suggesting the roles for OsNCED3 in response to the multi-abiotic stress tolerance in rice. Compared with wild-type plants, nced3 mutants had earlier seed germination, longer post-germination seedling growth, increased sensitivity to water stress and H2O2 stress and increased stomata aperture under water stress and delayed leaf senescence. Further analysis found that nced3 mutants contained lower ABA content compared with wild-type plants, overexpression of OsNCED3 in transgenic plants could enhance water stress tolerance, promote leaf senescence and increase ABA content. We conclude that OsNCED3 mediates seed dormancy, plant growth, abiotic stress tolerance, and leaf senescence by regulating ABA biosynthesis in rice; and may provide a new strategy for improving the quality of crop.

Heterosis, or hybrid vigor, refers to the phenomenon in which hybrid progeny of two inbred varieties exhibits enhanced growth or agronomic performance. Although a century-long history of research has generated several hypotheses regarding the genetic basis of heterosis, the molecular mechanisms underlying heterosis and heterotic gene expression remain elusive. Here, we report a genome-wide gene expression analysis of two heterotic crosses in rice, taking advantage of its fully sequenced genomes. Approximately 7-9% of the genes were differentially expressed in the seedling shoots from two sets of heterotic crosses, including many transcription factor genes, and exhibited multiple modes of gene action. Comparison of the putative promoter regions of the ortholog genes between inbred parents revealed extensive sequence variation, particularly small insertions/deletions (INDELs), many of which result in the formation/disruption of putative cis-regulatory elements. Together, these results suggest that a combinatorial interplay between expression of transcription factors and polymorphic promoter cis-regulatory elements in the hybrids is one plausible molecular mechanism underlying heterotic gene action and thus heterosis in rice.

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Heterosis, or hybrid vigor, is the phenomenon whereby progeny of two inbred lines exhibit superior agronomic performance compared with either parent. We analyzed the expression of miRNAs and highly expressed small RNAs (defined according to Solexa sequencing results) in two rice (Oryza sativa) subspecies (japonica cv. Nipponbare and indica cv. 93-11) and their reciprocal hybrids using microarrays. We found that of all the 1141 small RNAs tested, 140 (12%, 140 of 1141) and 157 (13%, 157 of 1141) were identified being significantly differentially expressed in two reciprocal hybrids, respectively. All possible modes of action, including additive, high-and low-parent, above high-and below low-parent modes were exhibited. Both F1 hybrids showed non-additive expression patterns, with downregulation predominating. Interestingly, 15 miRNAs displayed stark opposite expression trends relative to midparent in reciprocal hybrids. Computational prediction of targets of differentially expressed miRNAs showed that they participated in multifaceted developmental pathways, and were not distinguishable from the targets of non-differentially expressed miRNAs. Together, our findings reveal that small RNAs play roles in heterosis and add a new layer in the understanding and exploitation of molecular mechanisms of heterosis. Chen F, He G, He H, Chen W, Zhu X, Liang M, Chen L, Deng XW (2010) Expression analysis of miRNAs and highly-expressed small RNAs in two rice subspecies and their reciprocal hybrids. J. Integr. Plant Biol. 52(11), 971-980.