Functional classification, genomic organization, putatively cis-acting regulatory elements, and relationship to quantitative trait loci, of sorghum genes with rhizome-enriched expression

Abstract

Rhizomes are organs of fundamental importance to plant competitiveness and invasiveness. We have identified genes expressed at substantially higher levels in rhizomes than other plant parts, and explored their functional categorization, genomic organization, regulatory motifs, and association with quantitative trait loci (QTLs) conferring rhizomatousness. The finding that genes with rhizome-enriched expression are distributed across a wide range of functional categories suggests some degree of specialization of individual members of many gene families in rhizomatous plants. A disproportionate share of genes with rhizome-enriched expression was implicated in secondary and hormone metabolism, and abiotic stimuli and development. A high frequency of unknown-function genes reflects our still limited knowledge of this plant organ. A putative oligosaccharyl transferase showed the highest degree of rhizome-specific expression, with several transcriptional or regulatory protein complex factors also showing high (but lesser) degrees of specificity. Inferred by the upstream sequences of their putative rice (Oryza sativa) homologs, sorghum (Sorghum bicolor) genes that were relatively highly expressed in rhizome tip tissues were enriched for cis-element motifs, including the pyrimidine box, TATCCA box, and CAREs box, implicating the gibberellins in regulation of many rhizome-specific genes. From cDNA clones showing rhizome-enriched expression, expressed sequence tags forming 455 contigs were plotted on the rice genome and aligned to QTL likelihood intervals for ratooning and rhizomatous traits in rice and sorghum. Highly expressed rhizome genes were somewhat enriched in QTL likelihood intervals for rhizomatousness or ratooning, with specific candidates including some of the most rhizome-specific genes. Some rhizomatousness and ratooning QTLs were shown to be potentially related to one another as a result of ancient duplication, suggesting long-term functional conservation of the underlying genes. Insight into genes and pathways that influence rhizome growth set the stage for genetic and/or exogenous manipulation of rhizomatousness, and for further dissection of the molecular evolution of rhizomatousness.

Figure 1.

Associations between sorghum and rice rhizomatous and ratooning QTLs and candidate differentially expressed ESTs. Rice chromosome 1 and the corresponding sorghum QTL are shown in the printed volume; figures for the remaining chromosomes are available in Supplemental Figure S1. Comparative maps with QTLs by Hu et al. (2003) are modified according to physical data from TIGR release 2 rice pseudomolecules. In Figure 1 and/or its supplements, lines drawn to rice chromosome crossbars show BLASTn-supported locations of sorghum-rice anchor markers (as described in text). Additional anchor markers with inferred genetic positions based on either the Paterson et al. (1995) or high-density sorghum map (Bowers et al., 2003) are indicated by §. Loci added by BLASTn to the TIGR release 3 physical assembly are indicated by *. Anchor markers connected by dashed lines reflect changed positions, relative to the report by Hu et al. (2003), as determined based on the current rice pseudomolecules. ♦ indicates best BLASTn hits are to other genomic positions. Other observed discrepancies in colinearity of the Rice-IRRI RD23/Olong F2 QTL 2003 population mapped markers and the TIGR version 2 physical assembly are indicated by RM and OSR markers located to the right of the rice chromosome. For example, the physical map order of three markers, OSR13-OSR16-RM36, flanking the Rhz2 locus deviates from the genetic order of OSR16-RM36-OSR16.

Figure 2.

Ancient correspondence between rice paleohomeologous regions associated with rhizomatousness, tillering, and/or ratooning QTLs in rice and/or sorghum. Duplicated rice chromosomal regions were identified by synteny between protein-encoding genes reported by Paterson et al. (2004). For genetic marker positions, see “Materials and Methods” or Figure 1.