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. 2014 Feb 12:14:46.
doi: 10.1186/1471-2229-14-46.

A systems-wide comparison of red rice (Oryza longistaminata) tissues identifies rhizome specific genes and proteins that are targets for cultivated rice improvement

Ruifeng He, Fernanda Salvato, Jeong-Jin Park, Min-Jeong Kim, William Nelson, Tiago S Balbuena, Mark Willer, John A Crow, Greg D May, Carol A Soderlund, Jay J Thelen, David R Gang  1
Affiliations

A systems-wide comparison of red rice (Oryza longistaminata) tissues identifies rhizome specific genes and proteins that are targets for cultivated rice improvement

Ruifeng He et al. BMC Plant Biol. .

Abstract

Background: The rhizome, the original stem of land plants, enables species to invade new territory and is a critical component of perenniality, especially in grasses. Red rice (Oryza longistaminata) is a perennial wild rice species with many valuable traits that could be used to improve cultivated rice cultivars, including rhizomatousness, disease resistance and drought tolerance. Despite these features, little is known about the molecular mechanisms that contribute to rhizome growth, development and function in this plant.

Results: We used an integrated approach to compare the transcriptome, proteome and metabolome of the rhizome to other tissues of red rice. 116 Gb of transcriptome sequence was obtained from various tissues and used to identify rhizome-specific and preferentially expressed genes, including transcription factors and hormone metabolism and stress response-related genes. Proteomics and metabolomics approaches identified 41 proteins and more than 100 primary metabolites and plant hormones with rhizome preferential accumulation. Of particular interest was the identification of a large number of gene transcripts from Magnaportha oryzae, the fungus that causes rice blast disease in cultivated rice, even though the red rice plants showed no sign of disease.

Conclusions: A significant set of genes, proteins and metabolites appear to be specifically or preferentially expressed in the rhizome of O. longistaminata. The presence of M. oryzae gene transcripts at a high level in apparently healthy plants suggests that red rice is resistant to this pathogen, and may be able to provide genes to cultivated rice that will enable resistance to rice blast disease.

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Figures

Figure 1
Figure 1
Red rice (Oryza longistaminata ) plant and rhizome. (a) Plants (left) with strong rhizomes grow well in the greenhouse. The rhizome apical tips and the elongation zones of the rhizomes (right) were harvested for RNA, protein and metabolite isolation. (b) The anatomy of a cross section of the rhizome node. (c) A cross section of the rhizome internode.
Figure 2
Figure 2
Venn diagram showing unigene distribution among different tissues. A total of 3,187 unigenes were from rhizome only. A total of 31,842 unigenes were common to all four tissues: rhizome, root, stem and leaf.
Figure 3
Figure 3
Cytological and molecular analysis of M. oryzae in rhizome tissues. (a) Rhizome tissue sections were stained by Toluidine blue and visualized by light microscopy. Brown deposition/Rice blast lesions in individual epidermal cells were observed (arrow) but did not show spreading of the lesions on the rhizome tissue surface. Bar = 200 μm. (b) Fungal conidia were observed on the surface of rhizome (arrow) by scanning electron micrograph (SEM). Bar = 50 μm. (c) No fungal conidia or infection hyphae on red rice leaf tissues were detected. Bar = 100 μm. (d) The red rice plants grew in the greenhouse without any typical symptoms of rice blast/M. oryzae. (e) Fungal hyphae (arrow) spread on the Petri dish from the rhizome tissue with three days of culture on potao dextrose agar (PDA). (f) Fungal hyphae and spores (arrow) grew on the Petri dish from the rhizome tissue with eight days of culture on PDA. (g) An M. oryzae-specific gene was detected by RT-PCR, showing amplification of the predicted specific gene sequence 156 bp fragment in hyphyae/mycelia (lane 1) and rhizome (lane 2), but not in root (lane 3) and leaf (lane 4). L: DNA ladder.
Figure 4
Figure 4
Hierarchical clustering for the 119 rhizome-enriched genes.
Figure 5
Figure 5
Workflow for identification of red rice rhizome-characteristic proteins and differential regulation between the apical tip and the elongation zone proteins. Proportional venn diagram representing the total number of proteins identified in each Oryza longistaminata rhizome tissues before and after spectral count quantitative analysis. A total of 1747 proteins were identified and considered reproducible (detected in at least 3 biological replicates) in the rhizome apical tip, rhizome elongation zone and roots tissues. From this amount, 74, 15 and 288 proteins were exclusively detected in the tip, zone and root tissues, respectively. Differential expression was determined using the TFold test at p value of 0.05. Identifications that satisfied both fold and statistical criteria were considered differently regulated. After statistical analysis, we obtained 87 and 52 proteins up-regulated in tip and zone compared to roots, respectively. Proteins found to be up-regulated in both apical tip and elongation zone were combined to create a non-redundant list of the up-regulated, characteristic proteins. Differences between tip and zone were determined after removal of those detected in the same or lower expression level than in the roots.
Figure 6
Figure 6
Hierarchical clustering for the 41 rhizome-characteristic proteins (AT: apical tip; EZ: elongation zone; R: root).
Figure 7
Figure 7
Distribution of GO biological process and molecular function terms mapped for red rice rhizome proteins.
Figure 8
Figure 8
Hierarchical clustering analysis of 100 primary metabolites in red rice tissues. 100 primary metabolites from red rice rhizome apical tip, rhizome elongation zone, stem, leaf and root tissues, including 24 sugars, 32 organic acids, 20 amino acids and others were detected.
Figure 9
Figure 9
Comparative analysis of primary metabolites in different tissues of red rice. Amino acids were most abundant in rhizome tissue, especially in the tip compared to the other tissues.
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