Glycosyltransferases (GTs) (EC 2.4.x.y) catalyze the transfer of sugar moieties to a wide range of acceptor molecules, such as sugars, lipids, proteins, nucleic acids, antibiotics and other small ...molecules, including plant secondary metabolites. These enzymes can be classified into at least 92 families, of which family 1 glycosyltransferases (GT1), often referred to as UDP glycosyltransferases (UGTs), is the largest in the plant kingdom. To understand how UGTs expanded in both number and function during evolution of land plants, we screened genome sequences from six plants (Physcomitrella patens, Selaginella moellendorffii, Populus trichocarpa, Oryza sativa, Arabidopsis thaliana and Arabidopsis lyrata) for the presence of a conserved UGT protein domain. Phylogenetic analyses of the UGT genes revealed a significant expansion of UGTs, with lineage specificity and a higher duplication rate in vascular plants after the divergence of Physcomitrella. The UGTs from the six species fell into 24 orthologous groups that contained genes derived from the common ancestor of these six species. Some orthologous groups contained multiple UGT families with known functions, suggesting that UGTs discriminate compounds as substrates in a lineage-specific manner. Orthologous groups containing only a single UGT family tend to play a crucial role in plants, suggesting that such UGT families may have not expanded because of evolutionary constraints.
Water availability is a key determinant of terrestrial plant productivity. Many climate models predict that water stress will increasingly challenge agricultural yields and exacerbate projected food ...deficits. To ensure food security and increase agricultural efficiency, crop water productivity must be increased. Research over past decades has established that the phytohormone abscisic acid (ABA) is a central regulator of water use and directly regulates stomatal opening and transpiration. In this study, we investigated whether the water productivity of wheat could be improved by increasing its ABA sensitivity. We show that overexpression of a wheat ABA receptor increases wheat ABA sensitivity, which significantly lowers a plant's lifetime water consumption. Physiological analyses demonstrated that this water-saving trait is a consequence of reduced transpiration and a concomitant increase in photosynthetic activity, which together boost grain production per litre of water and protect productivity during water deficit. Our findings provide a general strategy for increasing water productivity that should be applicable to other crops because of the high conservation of the ABA signalling pathway.
Plants monitor the ambient light conditions using several informational photoreceptors, including red/far-red light absorbing phytochrome. Phytochrome is widely believed to regulate the transcription ...of light-responsive genes by modulating the activity of several transcription factors. Here we provide evidence that phytochrome significantly changes alternative splicing (AS) profiles at the genomic level in Arabidopsis , to approximately the same degree as it affects steady-state transcript levels. mRNA sequencing analysis revealed that 1,505 and 1,678 genes underwent changes in their AS and steady-state transcript level profiles, respectively, within 1 h of red light exposure in a phytochrome-dependent manner. Furthermore, we show that splicing factor genes were the main early targets of AS control by phytochrome, whereas transcription factor genes were the primary direct targets of phytochrome-mediated transcriptional regulation. We experimentally validated phytochrome-induced changes in the AS of genes that are involved in RNA splicing, phytochrome signaling, the circadian clock, and photosynthesis. Moreover, we show that phytochrome-induced AS changes of SPA1-RELATED 3 , the negative regulator of light signaling, physiologically contributed to promoting photomorphogenesis. Finally, photophysiological experiments demonstrated that phytochrome transduces the signal from its photosensory domain to induce light-dependent AS alterations in the nucleus. Taking these data together, we show that phytochrome directly induces AS cascades in parallel with transcriptional cascades to mediate light responses in Arabidopsis .
Significance Plants adapt to their fluctuating environment by monitoring surrounding light conditions through several photoreceptors, such as phytochrome. It is widely believed that upon absorbing red light, phytochrome induces plant light responses by regulating the transcription of numerous target genes. In this study, we provide clear evidence that phytochrome controls not only transcription, but also alternative splicing in Arabidopsis . We reveal that 6.9% of the annotated genes in the Arabidopsis genome undergo rapid changes in their alternative splicing patterns in a red light- and phytochrome-dependent manner. Our results demonstrate that phytochrome simultaneously regulates two different aspects of gene expression, namely transcription and alternative splicing to mediate light responses in plants.
Duplicated genes show various degrees of functional diversification in plants. We previously identified 1,052 pairs of high diversified duplicates (HDDs) and 600 pairs of low diversified duplicates ...(LDDs) in Arabidopsis thaliana. Single knock-down of HDDs induced abnormal phenotypic changes because the other gene copy could not compensate for the knock-down effect, while single knock-down of LDDs did not induce abnormal phenotypic changes because of functional compensation by the copy gene. Here, focusing on one pair each of HDDs and LDDs, we performed transcriptome analyses in single-knock-down transgenic plants. The numbers of differentially expressed genes in single-knock-down transgenic plants were not different between HDDs and LDDs. Thus, functional compensation inferred by transcriptomics was similar between HDDs and LDDs. However, the trend of differentially expressed genes was similar in the pair of LDDs, while expression profiles were dissimilar in the pair of HDDs. This result indicates that a pair of LDDs tends to share similar functions but a pair of HDDs tends to have undergone functional divergence. Taking these findings together, as the reason for no phenotypic changes in single knock-down of LDDs but phenotypic changes in double knock-down of LDDs, we concluded that phenotypic changes of LDDs were induced by decreasing gene dosage.
There is considerable diversity in the specialized metabolites within a single plant species (intra-species) and among different plant species (inter-species). The functional divergence associated ...with gene duplications largely contributes to the inter-species diversity in the specialized metabolites, whereas the intra-species diversity is due to gene dosage changes
gene duplications i.e., copy number variants (CNVs) at the intra-species level of evolution. This is because CNVs are thought to undergo associated with less functional divergence at the intra-species level of evolution. However, functional divergence caused by CNVs may induce specialized metabolite diversity at the intra-species and inter-species levels of evolution. We herein discuss the functional divergence of CNVs in metabolic quantitative trait genes (mQTGs). We focused on 5,654 previously identified mQTGs in 270
accessions. The ratio of nonsynonymous to synonymous variations tends to be higher for mQTGs with CNVs than for mQTGs without CNVs within
accessions, suggesting that CNVs are responsible for the functional divergence among mQTGs at the intra-species level of evolution. To evaluate the contribution of CNVs to inter-species diversity, we calculated the ratio of nonsynonymous to synonymous substitutions in the
lineage. The ratio tends to be higher for the mQTGs with CNVs than for the mQTGs without CNVs. Additionally, we determined that mQTGs with CNVs are subject to positive selection in the
lineage. Our data suggest that CNVs are closely related to functional divergence contributing to adaptations
the production of diverse specialized metabolites at the intra-species and inter-species levels of evolution.
Receptor-Like Kinase (RLK)/Pelle genes play roles ranging from growth regulation to defense response, and the dramatic expansion of this family has been postulated to be crucial for plant-specific ...adaptations. Despite this, little is known about the history of or the factors that contributed to the dramatic expansion of this gene family. In this study, we show that expansion coincided with the establishment of land plants and that RLK/Pelle subfamilies were established early in land plant evolution. The RLK/Pelle family expanded at a significantly higher rate than other kinases, due in large part to expansion of a few subfamilies by tandem duplication. Interestingly, these subfamilies tend to have members with known roles in defense response, suggesting that their rapid expansion was likely a consequence of adaptation to fast-evolving pathogens. Arabidopsis (Arabidopsis thaliana) expression data support the importance of RLK/Pelles in biotic stress response. We found that hundreds of RLK/Pelles are up-regulated by biotic stress. Furthermore, stress responsiveness is correlated with the degree of tandem duplication in RLK/Pelle subfamilies. Our findings suggest a link between stress response and tandem duplication and provide an explanation for why a large proportion of the RLK/Pelle gene family is found in tandem repeats. In addition, our findings provide a useful framework for potentially predicting RLK/Pelle stress functions based on knowledge of expansion pattern and duplication mechanism. Finally, we propose that the detection of highly variable molecular patterns associated with specific pathogens/parasites is the main reason for the up-regulation of hundreds of RLK/Pelles under biotic stress.
Alternative promoter usage is a proteome-expanding mechanism that allows multiple pre-mRNAs to be transcribed from a single gene. The impact of this mechanism on the proteome and whether it is ...positively exploited in normal organismal responses remain unclear. We found that the plant photoreceptor phytochrome induces genome-wide changes in alternative promoter selection in Arabidopsis thaliana. Through this mechanism, protein isoforms with different N termini are produced that display light-dependent differences in localization. For instance, shade-grown plants accumulate a cytoplasmic isoform of glycerate kinase (GLYK), an essential photorespiration enzyme that was previously thought to localize exclusively to the chloroplast. Cytoplasmic GLYK constitutes a photorespiratory bypass that alleviates fluctuating light-induced photoinhibition. Therefore, phytochrome controls alternative promoter selection to modulate protein localization in response to changing light conditions. This study suggests that alternative promoter usage represents another ubiquitous layer of gene expression regulation in eukaryotes that contributes to diversification of the proteome.
Display omitted
•Phytochrome induces genome-wide changes in alternative promoter selection•Phytochrome-mediated alternative promoter selection modulates protein localization•This mechanism produces a cytoplasmic isoform of glycerate kinase (cytGLYK)•cytGLYK accumulates in shade to alleviate fluctuating light-induced photoinhibition
Light signaling through phytochrome receptors changes protein localization through alternative promoter selection, allowing plants to metabolically respond to changing light conditions.
Plants have substantially higher gene duplication rates compared with most other eukaryotes. These plant gene duplicates are mostly derived from whole genome and/or tandem duplications. Earlier ...studies have shown that a large number of duplicate genes are retained over a long evolutionary time, and there is a clear functional bias in retention. However, the influence of duplication mechanism, particularly tandem duplication, on duplicate retention has not been thoroughly investigated. We have defined orthologous groups (OGs) between Arabidopsis (Arabidopsis thaliana) and three other land plants to examine the functional bias of retained duplicate genes during vascular plant evolution. Based on analysis of Gene Ontology categories, it is clear that genes in OGs that expanded via tandem duplication tend to be involved in responses to environmental stimuli, while those that expanded via nontandem mechanisms tend to have intracellular regulatory roles. Using Arabidopsis stress expression data, we further demonstrated that tandem duplicates in expanded OGs are significantly enriched in genes that are up-regulated by biotic stress conditions. In addition, tandem duplication of genes in an OG tends to be highly asymmetric. That is, expansion of OGs with tandem genes in one organismal lineage tends to be coupled with losses in the other. This is consistent with the notion that these tandem genes have experienced lineage-specific selection. In contrast, OGs with genes duplicated via nontandem mechanisms tend to experience convergent expansion, in which similar numbers of genes are gained in parallel. Our study demonstrates that the expansion of gene families and the retention of duplicates in plants exhibit substantial functional biases that are strongly influenced by the mechanism of duplication. In particular, genes involved in stress responses have an elevated probability of retention in a single-lineage fashion following tandem duplication, suggesting that these tandem duplicates are likely important for adaptive evolution to rapidly changing environments.
DNA methylation is an important factor regulating gene expression in organisms. However, whether DNA methylation plays a key role in adaptive evolution is unknown. Here, we show evidence of naturally ...selected DNA methylation in
In comparison with single nucleotide polymorphisms, three types of methylation-methylated CGs (mCGs), mCHGs, and mCHHs-contributed highly to variable gene expression levels among an
population. Such variably expressed genes largely affect a large variation of specialized metabolic quantities. Among the three types of methylations, only mCGs located in promoter regions of genes associated with specialized metabolites show a selective sweep signature in the
population. Thus, naturally selected mCGs appear to be key mutations that cause the expressional diversity associated with specialized metabolites during plant evolution.
Summary
To identify candidate genes involved in Arabidopsis flavonoid biosynthesis, we applied transcriptome coexpression analysis and independent component analyses with 1388 microarray data from ...publicly available databases. Two glycosyltransferases, UGT79B1 and UGT84A2 were found to cluster with anthocyanin biosynthetic genes. Anthocyanin was drastically reduced in ugt79b1 knockout mutants. Recombinant UGT79B1 protein converted cyanidin 3‐O‐glucoside to cyanidin 3‐O‐xylosyl(1→2)glucoside. UGT79B1 recognized 3‐O‐glucosylated anthocyanidins/flavonols and uridine diphosphate (UDP)‐xylose, but not 3,5‐O‐diglucosylated anthocyanidins, indicating that UGT79B1 encodes anthocyanin 3‐O‐glucoside: 2′′‐O‐xylosyltransferase. UGT84A2 is known to encode sinapic acid: UDP‐glucosyltransferase. In ugt84a2 knockout mutants, a major sinapoylated anthocyanin was drastically reduced. A comparison of anthocyanin profiles in ugt84a knockout mutants indicated that UGT84A2 plays a major role in sinapoylation of anthocyanin, and that other UGT84As contribute the production of 1‐O‐sinapoylglucose to a lesser extent. These data suggest major routes from cyanidin 3‐O‐glucoside to the most highly modified cyanidin in the potential intricate anthocyanin modification pathways in Arabidopsis.
PDF
