The tiller angle is an important agronomic trait that determines plant architecture and grain yield in rice (Oryza sativa L.). However, the molecular regulation mechanism of the rice tiller angle remains unclear. Here, we identified a rice tiller angle gene, LARGE TILLER ANGLE 1 (LATA1), using the MutMap approach. LATA1 encodes a C3H2C3-type RING zinc finger E3 ligase and the conserved region of the RING zinc finger is essential for its E3 activity. LATA1 was highly expressed in the root and tiller base and LATA1-GFP fusion protein was specifically localized to the nucleus. The mutation of LATA1 significantly reduced indole-3-acetic acid content and attenuated lateral auxin transport, thereby resulting in defective shoot gravitropism and spreading plant architecture in rice. Further investigations found that LATA1 may indirectly affect gravity perception by modulating the sedimentation rate of gravity-sensing amyloplasts upon gravistimulation. Our findings provide new insights into the molecular mechanism underlying the rice tiller angle and new genetic resource for the improvement of plant architecture in rice.

Tiller angle is a key agricultural trait that establishes plant architecture, which in turn strongly affects grain yield by influencing planting density in rice. The shoot gravity response plays a crucial role in the regulation of tiller angle in rice, but the underlying molecular mechanism is largely unknown. Here, we report the identification of the BIG TILLER ANGLE2 (BTA2), which regulates tiller angle by controlling the shoot gravity response in rice. Loss-of-function mutation of BTA2 dramatically reduced auxin content and affected auxin distribution in rice shoot base, leading to impaired gravitropism and therefore a big tiller angle. BTA2 interacted with AUXIN RESPONSE FACTOR7 (ARF7) to modulate rice tiller angle through the gravity signaling pathway. The BTA2 protein was highly conserved during evolution. Sequence variation in the BTA2 promoter of indica cultivars harboring a less expressed BTA2 allele caused lower BTA2 expression in shoot base and thus wide tiller angle during rice domestication. Overexpression of BTA2 significantly increased grain yield in the elite rice cultivar Huanghuazhan under appropriate dense planting conditions. Our findings thus uncovered the BTA2-ARF7 module that regulates tiller angle by mediating the shoot gravity response. Our work offers a target for genetic manipulation of plant architecture and valuable information for crop improvement by producing the ideal plant type.

Rice tiller angle is a key agronomic trait that has significant effects on the establishment of a high-yield rice population. However, the molecular mechanism underlying the control of rice tiller angle remains to be clarified. Here, we characterized the novel tiller-angle gene LAZY4 (LA4) in rice through map-based cloning. LA4 encodes a C3H2C3-type RING zinc-finger E3 ligase localized in the nucleus, and an in vitro ubiquitination assay revealed that the conserved RING finger domain is essential for its E3 ligase activity. We found that expression of LA4 can be induced by gravistimulation and that loss of LA4 function leads to defective shoot gravitropism caused by impaired asymmetric auxin redistribution upon gravistimulation. Genetic analysis demonstrated that LA4 acts in a distinct pathway from the starch biosynthesis regulators LA2 and LA3, which function in the starch-statolith-dependent pathway. Further genetic analysis showed that LA4 regulates shoot gravitropism and tiller angle by acting upstream of LA1 to mediate lateral auxin transport upon gravistimulation. Our studies reveal that LA4 regulates shoot gravitropism and tiller angle upstream of LA1 through a novel pathway independent of the LA2-LA3-mediated gravity-sensing mechanism, providing new insights into the rice tiller-angle regulatory network.

CONCLUSIONS: PROG1 is necessary but insufficient for the main culm inclination while TAC1 partially takes part in it, and both genes promote tiller inclination in Asian wild rice. Asian wild rice (Oryza rufipogon), the ancestor of cultivated rice (O. sativa), has a prostrate architecture, with tillers branching from near the ground. The main culm of each plant grows upward and then tilts during the vegetative stage. Genes controlling tiller angle have been reported; however, their genetic contributions to the culm movement have not been quantified. Here, we quantified their genetic contributions to angular kinematics in the main culm and tillers. For the main culm inclination, one major QTL surrounding the PROG1 region was found. In cultivated rice, tillers firstly inclined and lately rose, while it kept inclining in wild rice. It was suggested that PROG1 affected the tiller elevation angle in the later kinematics, whereas TAC1 was weakly associated with the tiller angle in the whole vegetative stage. Micro-computed tomography (micro-CT) suggested that these angular changes are produced by the bending of culm bases. Because near-isogenic lines (NILs) of wild rice-type Prog1 and Tac1 alleles in the genetic background of cultivated rice did not show the prostrate architecture, the involvement of another gene(s) for inclination of the main culm was suggested. Our findings will not only contribute to the understanding of the morphological transition during domestication but also be used in plant breeding to precisely reproduce the ideal plant architecture by combining the effects of multiple genes.

Rice flowering is triggered by transcriptional reprogramming at the shoot apical meristem (SAM) mediated by florigenic proteins produced in leaves in response to changes in photoperiod. Florigens are more rapidly expressed under short days (SDs) compared to long days (LDs) and include the HEADING DATE 3a (Hd3a) and RICE FLOWERING LOCUS T1 (RFT1) phosphatidylethanolamine binding proteins. Hd3a and RFT1 are largely redundant at converting the SAM into an inflorescence, but whether they activate the same target genes and convey all photoperiodic information that modifies gene expression at the SAM is currently unclear. We uncoupled the contribution of Hd3a and RFT1 to transcriptome reprogramming at the SAM by RNA sequencing of dexamethasone-inducible over-expressors of single florigens and wild-type plants exposed to photoperiodic induction. Fifteen highly differentially expressed genes common to Hd3a, RFT1, and SDs were retrieved, 10 of which still uncharacterized. Detailed functional studies on some candidates revealed a role for LOC_Os04g13150 in determining tiller angle and spikelet development and the gene was renamed BROADER TILLER ANGLE 1 (BRT1). We identified a core set of genes controlled by florigen-mediated photoperiodic induction and defined the function of a novel florigen target controlling tiller angle and spikelet development.

Starch biosynthesis in gravity-sensing tissues of rice shoot determines the magnitude of rice shoot gravitropism and thus tiller angle. However, the molecular mechanism underlying starch biosynthesis in rice gravity-sensing tissues is still unclear. We characterized a novel tiller angle gene LAZY3 (LA3) in rice through map-based cloning. Biochemical, molecular and genetic studies further demonstrated the essential roles of LA3 in gravity perception of rice shoot and tiller angle control. The shoot gravitropism and lateral auxin transport were defective in la3 mutant upon gravistimulation. We showed that LA3 encodes a chloroplast-localized tryptophan-rich protein associated with starch granules via Tryptophan-rich region (TRR) domain. Moreover, LA3 could interact with the starch biosynthesis regulator LA2, determining starch granule formation in shoot gravity-sensing tissues. LA3 and LA2 negatively regulate tiller angle in the same pathway acting upstream of LA1 to mediate asymmetric distribution of auxin. Our study defined LA3 as an indispensable factor of starch biosynthesis in rice gravity-sensing tissues that greatly broadens current understanding in the molecular mechanisms underlying the starch granule formation in gravity-sensing tissues, and provides new insights into the regulatory mechanism of shoot gravitropism and rice tiller angle.

Tiller angle is one of the most important agronomic traits and one key factor for wheat ideal plant architecture, which can both increase photosynthetic efficiency and greatly enhance grain yield. Here, a deacetylase HST1-like (TaHST1L) gene controlling wheat tiller angle was identified by the combination of a genome-wide association study (GWAS) and bulked segregant analysis (BSA). Ethyl methane sulfonate (EMS)-mutagenized tetraploid wheat lines with the premature stop codon of TaHST1L exhibited significantly smaller tiller angles than the wild type. TaHST1L-overexpressing (OE) plants exhibited significantly larger tiller angles and increased tiller numbers in both winter and spring wheat, while TaHST1L-silenced RNAi plants displayed significantly smaller tiller angles and decreased tiller numbers. Moreover, TaHST1L strongly interacted with TaIAA17 and inhibited its expression at the protein level, and thus possibly improved the content of endogenous auxin in the basal tissue of tillers. The transcriptomics and metabolomics results indicated that TaHST1L might change plant architecture by mediating auxin signal transduction and regulating endogenous auxin levels. In addition, a 242-bp insertion/deletion (InDel) in the TaHST1L-A1 promoter altered transcriptional activity and TaHST1L-A1b allele with the 242-bp insertion widened the tiller angle of TaHST1L-OE transgenic rice plants. Wheat varieties with TaHST1L-A1b allele possessed the increased tiller angle and grain yield. Further analysis in wheat and its progenitors indicated that the 242-bp InDel possibly originated from wild emmer and was strongly domesticated in the current varieties. Therefore, TaHST1L involved in the auxin signalling pathway showed the big potential to improve wheat yield by controlling plant architecture.

Tiller angle is an important trait that determines plant architecture and yield in cereal crops. Tiller angle is partially controlled during gravistimulation by the dynamic re-allocation of LAZY1 (LA1) protein between the nucleus and plasma membrane, but the underlying mechanism remains unclear. In this study, we identified and characterized a new allele of LA1 based on analysis of a rice (Oryza sativa L.) spreading-tiller mutant la1G74V, which harbors a non-synonymous mutation in the predicted transmembrane (TM) domain-encoding region of this gene. The mutation causes complete loss of shoot gravitropism, leading to prostrate growth of plants. Our results showed that LA1 localizes not only to the nucleus and plasma membrane but also to the endoplasmic reticulum. Removal of the TM domain in LA1 showed spreading-tiller phenotype of plants similar to la1G74V but did not affect the plasma membrane localization; thus, making it distinct from its ortholog ZmLA1 in Zea mays. Therefore, we propose that the TM domain is indispensable for the biological function of LA1, but this domain does not determine the localization of the protein to the plasma membrane. Our study provides new insights into the LA1-mediated regulation of shoot gravitropism.

CONCLUSIONS: Novel alleles of two reported tiller angle genes and eleven candidate genes for rice tiller angle were identified by combining GWAS with transcriptomic, qRT-PCR and haplotype analysis. Rice tiller angle is a key agronomic trait determining rice grain yield. Several quantitative trait loci (QTLs) affecting rice tiller angle have been mapped in the past decades. Little is known about the genetic base of tiller angle in rice, because rice tiller angle is a complex polygenic trait. In this study, we performed genome-wide association study (GWAS) on tiller angle in rice using a population of 164 japonica varieties derived from the 3 K Rice Genomes Project (3 K RGP). We detected a total of 18 QTLs using 1135519 single-nucleotide polymorphisms (SNP) based on three GWAS models (GLM, FastLMM and FarmCPU). Among them, two identified QTLs, qTA8.3 and qTA8.4, overlapped with PAY1 and TIG1, respectively, and additional 16 QTLs were identified for the first time. Combined with haplotype and expression analyses, we further revealed that PAY1 harbors one non-synonymous variation at its coding region, likely leading to variable tiller angle in the population, and that nature variations in the promoter of TIG1 significantly affect its expression, closely correlating with tiller angle phenotypes observed. Similarly, using qRT-PCR and haplotype analysis, we identified 1 and 7 candidate genes in qTA6.1 and qTA8.1 that were commonly detected by two GWAS models, respectively. In addition, we identified 3 more candidate genes in the remaining 14 novel QTLs after filtering by transcriptome analysis and qRT-PCR. In summary, this study provides new insights into the genetic architecture of rice tiller angle and candidate genes for rice breeding.

An ideal plant architecture is an important condition to achieve high crop yields. The tiller angle is an important and complex polygenic trait of rice (Oryza sativa L.) plant architecture. Therefore, the discovery and identification of tiller angle-related genes can aid in the improvement of crop architecture and yield. In the present study, 222 SSR markers were used to establish a high-density genetic map of rice doubled haploid population, and a total of 8 quantitative trait loci (QTLs) were detected based on the phenotypic data of the tiller angle and tiller crown width over 2 years. Among them, four QTLs (qTA9, qCW9, qTA9-1, and qCW9-1) were overlapped at marker interval RM6235-RM24288 on chromosome 9 with a large effect value regarded as a stable major QTL. The selected promising related genes were further identified by relative gene expression analysis, which gives us a basis for the future cloning of these genes. Finally, OsSAURq9, which belongs to the SMALL AUXIN UP RNA (SAUR), an auxin-responsive protein family, was selected as a target gene. Overall, this work will help broaden our knowledge of the genetic control of tiller angle and tiller crown width, and this study provides both a good theoretical basis and a new genetic resource for the breeding of ideal-type rice.