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A Systematic View of the MLO Family in Rice Suggests Their Novel Roles in Morphological Development, Diurnal Responses, the Light-Signaling Pathway, and Various Stress Responses

View Article: PubMed Central - PubMed

ABSTRACT

The Mildew resistance Locus O (MLO) family is unique to plants, containing genes that were initially identified as a susceptibility factor to powdery mildew pathogens. However, little is known about the roles and functional diversity of this family in rice, a model crop plant. The rice genome has 12 potential MLO family members. To achieve systematic functional assignments, we performed a phylogenomic analysis by integrating meta-expression data obtained from public sources of microarray data and real-time expression data into a phylogenic tree. Subsequently, we identified 12 MLO genes with various tissue-preferred patterns, including leaf, root, pollen, and ubiquitous expression. This suggested their functional diversity for morphological agronomic traits. We also used these integrated transcriptome data within a phylogenetic context to estimate the functional redundancy or specificity among OsMLO family members. Here, OsMLO12 showed preferential expression in mature pollen; OsMLO4, in the root tips; OsMLO10, throughout the roots except at the tips; and OsMLO8, expression preferential to the leaves and trinucleate pollen. Of particular interest to us was the diurnal expression of OsMLO1, OsMLO3, and OsMLO8, which indicated that they are potentially significant in responses to environmental changes. In osdxr mutants that show defects in the light response, OsMLO1, OsMLO3, OsMLO8, and four calmodulin genes were down-regulated. This finding provides insight into the novel functions of MLO proteins associated with the light-responsive methylerythritol 4-phosphate pathway. In addition, abiotic stress meta-expression data and real-time expression analysis implied that four and five MLO genes in rice are associated with responses to heat and cold stress, respectively. Upregulation of OsMLO3 by Magnaporthe oryzae infection further suggested that this gene participates in the response to pathogens. Our analysis has produced fundamental information that will enhance future studies of the diverse developmental or physiological phenomena mediated by the MLO family in this model plant system.

No MeSH data available.


Meta-analysis of OsMLO gene expression patterns using 983 Affymetrix anatomical array data. Blue, low level of log2 intensity; yellow, high level. Gray bar, indica samples; black bar, japonica samples. OsMLO11 has no probe on rice Affymetrix chip. SAM, shoot apical meristem; PMe, pre-meiotic; Me, meiotic; Uni, uninucleate stage; Bi, binucleate stage; Tri, trinucleate stage; DAP, days after pollination.
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Figure 1: Meta-analysis of OsMLO gene expression patterns using 983 Affymetrix anatomical array data. Blue, low level of log2 intensity; yellow, high level. Gray bar, indica samples; black bar, japonica samples. OsMLO11 has no probe on rice Affymetrix chip. SAM, shoot apical meristem; PMe, pre-meiotic; Me, meiotic; Uni, uninucleate stage; Bi, binucleate stage; Tri, trinucleate stage; DAP, days after pollination.

Mentions: Using protein sequences for 12 MLO genes in rice, we generated a phylogenetic tree that incorporated subgroup information and anatomical meta-expression profiles based on 983 Affymetrix array data (Cao et al., 2012) (Figure 1). Starting at the top of the tree, OsMLO3 displayed a medium level of expression in almost all tissues, including roots, shoots, leaves, and flag leaves at the vegetative stage, and anthers and seeds at the reproductive stage. It was most closely linked with OsMLO6. However, very low expression by the latter in whole tissues suggested that OsMLO3 had a more dominant role. Uniquely, OsMLO12 showed strong anther-preferred expression in trinucleate and mature pollen. This profile was consistent with that reported by Yi et al. (2014). Expression of OsMLO1 was high in anthers at the uninucleate stage, especially in indica rice, although not at a level similar to that found in uninucleate pollen (Figure S1). Thus, OsMLO1 might be more active in the anthers than in the pollen grains themselves. The Affymetrix data revealed that OsMLO4 was preferentially expressed in the root tips but at only a low level in other tissues. In contrast, OsMLO2 was ubiquitously expressed. One of its paralogs, OsMLO9, showed dominant expression patterns in reproductive organs, and transcripts were particularly abundant in anthers at the uninucleate pollen stage while OsMLO2 was not detected there (Figure S1). Although OsMLO5 and OsMLO10, as well as OsMLO7 and OsMLO8, are thought to have resulted from segmental duplication, each pairing appears to have retained differential expression patterns from an anatomical perspective. While expression of OsMLO5 was extremely low in the roots, that of OsMLO10 was much higher than for OsMLO5. Moreover, when compared with OsMLO7, OsMLO8 was more predominantly expressed in the shoots, leaves, and anthers at the trinucleate pollen stage (Figure 1). All of these findings suggested that functional specificity and dominance is much greater for OsMLO8 and OsMLO10 than for their homologs OsMLO7 and OsMLO5, respectively. Therefore, with the exception of OsMLO11, for which no probe was printed on the Affymetrix chip, we were able to use meta-expression data to estimate the anatomical functions of all MLO genes examined here.


A Systematic View of the MLO Family in Rice Suggests Their Novel Roles in Morphological Development, Diurnal Responses, the Light-Signaling Pathway, and Various Stress Responses
Meta-analysis of OsMLO gene expression patterns using 983 Affymetrix anatomical array data. Blue, low level of log2 intensity; yellow, high level. Gray bar, indica samples; black bar, japonica samples. OsMLO11 has no probe on rice Affymetrix chip. SAM, shoot apical meristem; PMe, pre-meiotic; Me, meiotic; Uni, uninucleate stage; Bi, binucleate stage; Tri, trinucleate stage; DAP, days after pollination.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5037229&req=5

Figure 1: Meta-analysis of OsMLO gene expression patterns using 983 Affymetrix anatomical array data. Blue, low level of log2 intensity; yellow, high level. Gray bar, indica samples; black bar, japonica samples. OsMLO11 has no probe on rice Affymetrix chip. SAM, shoot apical meristem; PMe, pre-meiotic; Me, meiotic; Uni, uninucleate stage; Bi, binucleate stage; Tri, trinucleate stage; DAP, days after pollination.
Mentions: Using protein sequences for 12 MLO genes in rice, we generated a phylogenetic tree that incorporated subgroup information and anatomical meta-expression profiles based on 983 Affymetrix array data (Cao et al., 2012) (Figure 1). Starting at the top of the tree, OsMLO3 displayed a medium level of expression in almost all tissues, including roots, shoots, leaves, and flag leaves at the vegetative stage, and anthers and seeds at the reproductive stage. It was most closely linked with OsMLO6. However, very low expression by the latter in whole tissues suggested that OsMLO3 had a more dominant role. Uniquely, OsMLO12 showed strong anther-preferred expression in trinucleate and mature pollen. This profile was consistent with that reported by Yi et al. (2014). Expression of OsMLO1 was high in anthers at the uninucleate stage, especially in indica rice, although not at a level similar to that found in uninucleate pollen (Figure S1). Thus, OsMLO1 might be more active in the anthers than in the pollen grains themselves. The Affymetrix data revealed that OsMLO4 was preferentially expressed in the root tips but at only a low level in other tissues. In contrast, OsMLO2 was ubiquitously expressed. One of its paralogs, OsMLO9, showed dominant expression patterns in reproductive organs, and transcripts were particularly abundant in anthers at the uninucleate pollen stage while OsMLO2 was not detected there (Figure S1). Although OsMLO5 and OsMLO10, as well as OsMLO7 and OsMLO8, are thought to have resulted from segmental duplication, each pairing appears to have retained differential expression patterns from an anatomical perspective. While expression of OsMLO5 was extremely low in the roots, that of OsMLO10 was much higher than for OsMLO5. Moreover, when compared with OsMLO7, OsMLO8 was more predominantly expressed in the shoots, leaves, and anthers at the trinucleate pollen stage (Figure 1). All of these findings suggested that functional specificity and dominance is much greater for OsMLO8 and OsMLO10 than for their homologs OsMLO7 and OsMLO5, respectively. Therefore, with the exception of OsMLO11, for which no probe was printed on the Affymetrix chip, we were able to use meta-expression data to estimate the anatomical functions of all MLO genes examined here.

View Article: PubMed Central - PubMed

ABSTRACT

The Mildew resistance Locus O (MLO) family is unique to plants, containing genes that were initially identified as a susceptibility factor to powdery mildew pathogens. However, little is known about the roles and functional diversity of this family in rice, a model crop plant. The rice genome has 12 potential MLO family members. To achieve systematic functional assignments, we performed a phylogenomic analysis by integrating meta-expression data obtained from public sources of microarray data and real-time expression data into a phylogenic tree. Subsequently, we identified 12 MLO genes with various tissue-preferred patterns, including leaf, root, pollen, and ubiquitous expression. This suggested their functional diversity for morphological agronomic traits. We also used these integrated transcriptome data within a phylogenetic context to estimate the functional redundancy or specificity among OsMLO family members. Here, OsMLO12 showed preferential expression in mature pollen; OsMLO4, in the root tips; OsMLO10, throughout the roots except at the tips; and OsMLO8, expression preferential to the leaves and trinucleate pollen. Of particular interest to us was the diurnal expression of OsMLO1, OsMLO3, and OsMLO8, which indicated that they are potentially significant in responses to environmental changes. In osdxr mutants that show defects in the light response, OsMLO1, OsMLO3, OsMLO8, and four calmodulin genes were down-regulated. This finding provides insight into the novel functions of MLO proteins associated with the light-responsive methylerythritol 4-phosphate pathway. In addition, abiotic stress meta-expression data and real-time expression analysis implied that four and five MLO genes in rice are associated with responses to heat and cold stress, respectively. Upregulation of OsMLO3 by Magnaporthe oryzae infection further suggested that this gene participates in the response to pathogens. Our analysis has produced fundamental information that will enhance future studies of the diverse developmental or physiological phenomena mediated by the MLO family in this model plant system.

No MeSH data available.