SignificanceRice architecture is an important agronomic trait for determining yield; however, the complexity of this trait makes it difficult to elucidate the molecular mechanisms. This study applied a strategy of using principal components (PCs) as dependent variables for a genome-wide association study (GWAS). SPINDLY was identified to regulate rice architecture by suppressing gibberellin (GA) signaling. Further study using GA-signaling mutants confirmed that levels of GA responsiveness regulate rice architecture, suggesting that the utilization of a favorable SPINDLY allele will improve crop productivity. The strategy presented in this study of performing GWAS using PC scores will provide valuable information for plant genetics and will improve our understanding of complex traits at the molecular level.
SignificanceThe plant gibberellin receptor GID1 shows sequence similarity to carboxylesterase, suggesting that it is derived from an enzyme. However, how GID1 evolved and was modified is unclear. We identified two amino acids that are essential for GID1 activity, and we found that adjustment of these residues caused GID1 to recognize novel GAs carrying 13-OH as active GAs and to strictly refuse inactive GAs. Phylogenetic analysis of 169 GID1s revealed seven subtypes, and the B-type in core eudicots showed unique characteristics. In fact, certain B-type GID1s showed a higher nonsynonymous-to-synonymous divergence ratio in the region determining GA affinity. Such B-type GID1s with higher affinity were preferentially expressed in the roots in some core eudicot plants and conferred adaptive growth under stress.
Some ferns possess the ability to control their sex ratio to maintain genetic variation in their colony with the aid of antheridiogen pheromones, antheridium (male organ)-inducing compounds that are related to gibberellin. We determined that ferns have evolved an antheridiogen-mediated communication system to produce males by modifying the gibberellin biosynthetic pathway, which is split between two individuals of different developmental stages in the colony. Antheridiogen acts as a bridge between them because it is more readily taken up by prothalli than bioactive gibberellin. The pathway initiates in early-maturing prothalli (gametophytes) within a colony, which produce antheridiogens and secrete them into the environment. After the secreted antheridiogen is absorbed by neighboring late-maturing prothalli, it is modified in to bioactive gibberellin to trigger male organ formation.
Translocation and long-distance transport of phytohormones are considered important processes for phytohormone responses as well as their synthesis and signaling. Here, we report on the dual function of OsSWEET3a, a bidirectional sugar transporter from Clade I of the rice SWEET family of proteins, as both a gibberellin (GA) and a glucose transporter. OsSWEET3a efficiently transports GAs in the C13-hydroxylation pathway of GA biosynthesis. Both knockout and overexpression lines of OsSWEET3a showed defects in germination and early shoot development, which were partially restored by GA, especially GA20. Quantitative reverse transcription PCR, GUS staining, and in situ hybridization revealed that OsSWEET3a was expressed in vascular bundles in basal parts of the seedlings. OsSWEET3a expression co-localized with OsGA20ox1 expression in the vascular bundles but not with OsGA3ox2, whose expression was restricted to leaf primordia and young leaves. These results suggest that OsSWEET3a is expressed in the vascular tissue of basal parts of seedlings and is involved in the transport of both GA20 and glucose to young leaves, where GA20 is possibly converted to the bioactive GA1 form by OsGA3ox2, during early plant development. We also indicated that such GA transport activities of SWEET proteins have sporadically appeared in the evolution of plants: GA transporters in Arabidopsis evolved from sucrose transporters, while those in rice and sorghum have evolved from glucose transporters.
Allosteric regulation is protein activation by effector binding at a site other than the active site. Here, we show via X-ray structural analysis of gibberellin 2-oxidase 3 (GA2ox3), and auxin dioxygenase (DAO), that such a mechanism maintains hormonal homeostasis in plants. Both enzymes form multimers by interacting via GA4 and indole-3-acetic acid (IAA) at their binding interface. Via further functional analyses we reveal that multimerization of these enzymes gradually proceeds with increasing GA4 and IAA concentrations; multimerized enzymes have higher specific activities than monomer forms, a system that should favour the maintenance of homeostasis for these phytohormones. Molecular dynamic analysis suggests a possible mechanism underlying increased GA2ox3 activity by multimerization—GA4 in the interface of oligomerized GA2ox3s may be able to enter the active site with a low energy barrier. In summary, homeostatic systems for maintaining GA and IAA levels, based on a common allosteric mechanism, appear to have developed independently.
Previously, we found 123 transcription factors (TFs) as candidate regulators of secondary cell wall (SCW) formation in rice by using phylogenetic and co-expression network analyses. Among them, we examined in this work the role of OsIDD2, a zinc finger and indeterminate domain (IDD) family TF. Its overexpressors showed dwarfism, fragile leaves, and decreased lignin content, which are typical phenotypes of plants defective in SCW formation, whereas its knockout plants showed slightly increased lignin content. The RNA-seq and quantitative reverse transcription polymerase chain reaction analyses confirmed that some lignin biosynthetic genes were downregulated in the OsIDD2-overexpressing plants, and revealed the same case for other genes involved in cellulose synthesis and sucrose metabolism. The transient expression assay using rice protoplasts revealed that OsIDD2 negatively regulates the transcription of genes involved in lignin biosynthesis, cinnamyl alcohol dehydrogenase 2 and 3 (CAD2 and 3), and sucrose metabolism, sucrose synthase 5 (SUS5), whereas an AlphaScreen assay, which can detect the interaction between TFs and their target DNA sequences, directly confirmed the interaction between OsIDD2 and the target sequences located in the promoter regions of CAD2 and CAD3. Based on these observations, we conclude that OsIDD2 is negatively involved in SCW formation and other biological events by downregulating its target genes.
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