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. 2008 Nov;3(11):1024–1025. doi: 10.4161/psb.6770

Small RNA regulation of rice homeobox genes

Mukesh Jain 1,✉, Jitendra P Khurana 2
PMCID: PMC2633765  PMID: 19704442

Abstract

Recently, we reported the genome-wide identification of 107 homeobox genes in rice and classified them into ten distinct subfamilies based upon their domain composition and phylogenetic analysis. Microarray analysis revealed the tissue-specific and overlapping expression profiles of these genes during various stages of floral transition, panicle development and seed set. Several homeobox genes were also found to be differentially expressed under abiotic stress conditions. Based on massively parallel signature sequencing (MPSS) data analysis, we report here that a large number of small RNA signatures are associated with rice homeobox genes, which may be involved in their tissue-specific/developmental regulation and stress responses. The association of a very large number of small RNA signatures suggested an unusually high degree of regulation of homeobox genes by small RNAs during inflorescence development.

Key words: homeobox genes, small RNA, microRNA, rice (Oryza sativa), developmental regulation, stress response

The homeobox genes are key regulators of cell fate and body plan specification at the early stage of embryogenesis in higher organisms. The plant homeobox genes have been implicated in various developmental processes, such as embryo patterning, development of root, shoot and floral meristems, vascular development and hormone and stress responses as well.1–6 The homeobox genes have been catalogued into different groups based on the amino acid sequence of homeodomain and presence of their conserved motifs.1,7 Recently, we identified 107 homeobox genes in rice and reported that many of these genes display differential expression during various stages of reproductive development and abiotic stress conditions.7

Small RNA (21–24 nucleotides in length), including short interfering RNAs (siRNAs) and microRNAs (miRNAs), target specific complementary mRNAs to regulate their expression in extremely specific manner. The importance of small RNAs in controlling plant development has been well documented.8–11 Recently, adopting MPSS technology, nearly three million small RNAs representing three tissue-specific libraries (seedling leaf, stem and inflorescence) and about 1.5 million small RNAs from control seedlings and seedlings treated with abscisic acid and germinating seedlings of rice infected with Magnaporthe grisea (strain 70–15) have been sequenced (http://mpss.udel.edu/rice/); these small RNA sequences, available in the database, match repetitive sequences, intergenic regions and genes, indicating an extensive and complex repertoire of these molecules.12 We searched this dataset for the presence of small RNAs corresponding to the homeobox genes using the Rice MPSS Project browser. Out of 107, the small RNA signatures could be associated with 95 homeobox genes in at least one of the libraries. Among these, at least 85 homeobox genes have three or more tpq (tags per quarter million) in at least one library (Table S1). The number of small RNAs corresponding to these genes varied greatly in the tissuespecific libraries, indicating the tissue-specific and/or developmental regulation of their expression (Fig. 1; Table S1). The inflorescence library produced the greatest number of small RNAs corresponding to homeobox genes (ca 139 small RNAs per gene) as compared to stem (ca 46 small RNAs per gene) and young leaf (ca 25 small RNAs per gene) libraries. This observation is in sharp contrast to the results from analysis of whole library data, which showed the greatest number of small RNA clusters in stem libraries and their substantial reduction in the inflorescence.12 These results suggest an unusually high degree of small RNA regulation of homeobox genes during inflorescence development. A large number of small RNA signatures from MPSS libraries of seedlings treated with plant stress hormone abscisic acid and seedlings infected with Magnaporthe grisea were also found to be associated with rice homeobox genes (Fig. 1; Table S1), indicating their role in abiotic and biotic stress responses.

Figure 1.

Figure 1

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Heatmap showing the number of small RNA signatures associated with rice homeobox genes based on MPSS data. The number of significant signatures in terms of tags per quarter million (tpq) are shown. The color scale (representing tpq) is shown at the bottom. STM, stem; SNU, germinating seedlings; FLR, 90 days immature panicle; SNM, Germinating seedlings infected with Magnaporthe grisea (strain 70–15); ABA, seedlings treated with abscisic acid; UNT, control seedlings for abscisic acid treatment.

In Arabidopsis, the members of HD-ZIP III subfamily, PHB, PHV, REV, ATHB8 and ATHB15, have been predicted to be the targets of miRNAs.13 The miRNA-mediated regulation of PHB and PHV controls the transcriptional program that establishes adaxialabaxial polarity.14 Our analyses show that a significant number of small RNAs in rice are associated with about 80% of homeobox genes, representing members of all subfamilies. Many of these small RNAs may represent novel miRNAs, which target specific homeobox genes to control their expression. It has been reported that miRNAs have the potential to be produced from different loci. For example, miR165/166, which target PHB, PHV, REV, ATHB8 and ATHB15 HD-ZIP III family homeobox genes in Arabidopsis, have the potential to be produced from nine different loci and these loci may have different temporal and spatial expression patterns.15 The small RNAs associated with rice homeobox genes identified in this study also originated from different loci in the rice genome and may be important for the tissue-specific/developmental regulation and stress responses of their target homeobox genes. Taken together, these results suggest that several rice homeobox genes are putative targets of small RNAs, which control various aspects of plant growth and development. The evaluation of contribution of small RNAs and/or miRNAs towards regulation of homeobox genes is the subject of future research.

Note

Supplementary materials can be found at: www.landesbioscience.com/supplement/JainPSB3-11-Sup.pdf

Addendum to: Jain M, Tyagi AK, Khurana JP. Genome-wide identification, classification, evolutionary expansion, and expression analyses of homeobox genes in rice. FEBS J. 2008;275:2845–2861. doi: 10.1111/j.1742-4658.2008.06424.x.

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: www.landesbioscience.com/journals/psb/article/6770

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