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.

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.

BACKGROUND: In plants, gravity directs bidirectional growth; it specifies upward growth of shoots and downward growth of roots. Due to gravity, roots establish robust anchorage and shoot, which enables to photosynthesize. It sets optimum posture and develops plant architecture to efficiently use resources like water, nutrients, CO2, and gaseous exchange. Hence, gravitropism is crucial for crop productivity as well as for the growth of plants in challenging climate. Some SGR members are known to affect tiller and shoot angle, organ size, and inflorescence stem in plants.
OBJECTIVE: Although the SHOOT GRAVITROPISM (SGR) family plays a key role in regulating the fate of shoot gravitropism, little is known about its function compared to other proteins involved in gravity response in plant cells and tissues. Moreover, less information on the SGR family\'s physiological activities and biochemical responses in shoot gravitropism is available. This review scrutinizes and highlights the recent developments in shoot gravitropism and provides an outlook for future crop development, multi-application scenarios, and translational research to improve agricultural productivity.
UNASSIGNED: Plants have evolved multiple gene families specialized in gravitropic responses, of which the SGR family is highly significant. The SGR family regulates the plant\'s gravity response by regulating specific physiological and biochemical processes such as transcription, cell division, amyloplast sedimentation, endodermis development, and vacuole formation. Here, we analyze the latest discoveries in shoot gravitropism with particular attention to SGR proteins in plant cell biology, cellular physiology, and homeostasis. Plant cells detect gravity signals by sedimentation of amyloplast (starch granules) in the direction of gravity, and the signaling cascade begins. Gravity sensing, signaling, and auxin redistribution (organ curvature) are the three components of plant gravitropism. Eventually, we focus on the role of multiple SGR genes in shoot and present a complete update on the participation of SGR family members in gravity.

Identifying the genetic architecture underlying adaptive traits is exceptionally challenging in natural populations. This is because associations between traits not only mask the targets of selection but also create correlated patterns of genomic divergence that hinder our ability to isolate causal genetic effects. Here, we examine the repeated evolution of components of the auxin pathway that have contributed to the replicated loss of gravitropism (i.e. the ability of a plant to bend in response to gravity) in multiple populations of the Senecio lautus species complex in Australia. We use a powerful approach which combines parallel population genomics with association mapping in a Multiparent Advanced Generation Inter-Cross (MAGIC) population to break down genetic and trait correlations to reveal how adaptive traits evolve during replicated evolution. We sequenced auxin and shoot gravitropism-related gene regions in 80 individuals from six natural populations (three parallel divergence events) and 133 individuals from a MAGIC population derived from two of the recently diverged natural populations. We show that artificial tail selection on gravitropism in the MAGIC population recreates patterns of parallel divergence in the auxin pathway in the natural populations. We reveal a set of 55 auxin gene regions that have evolved repeatedly during the evolution of the species, of which 50 are directly associated with gravitropism divergence in the MAGIC population. Our work creates a strong link between patterns of genomic divergence and trait variation contributing to replicated evolution by natural selection, paving the way to understand the origin and maintenance of adaptations in natural populations.

Plant shoot gravitropism is a complex phenomenon resulting from gravity sensing, curvature sensing (proprioception), the ability to uphold self-weight and growth. Although recent data analysis and modelling have revealed the detailed morphology of shoot bending, the relative contribution of bending force (derived from the gravi-proprioceptive response) and stretching force (derived from shoot axial growth) behind gravitropism remains poorly understood. To address this gap, we combined morphological data with a theoretical model to analyze shoot bending in wild-type and lazy1-like 1 mutant Arabidopsis thaliana. Using data from actual bending events, we searched for model parameters that minimized discrepancies between the data and mathematical model. The resulting model suggests that both the bending force and the stretching force differ significantly between the wild type and mutant. We discuss the implications of the mechanical forces associated with differential cell growth and present a plausible mechanical explanation of shoot gravitropism.

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 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.

Crop plant architecture is an important agronomic trait that contributes greatly to crop yield. Tiller angle is one of the most critical components that determine crop plant architecture, which in turn substantially affects grain yield mainly owing to its large influence on plant density. Gravity is a fundamental physical force that acts on all organisms on earth. Plant organs sense gravity to control their growth orientation, including tiller angle in rice (Oryza sativa). This review summarizes recent research advances made using rice tiller angle as a research model, providing insights into domestication of rice tiller angle, genetic regulation of rice tiller angle, and shoot gravitropism. Finally, we propose that current discoveries in rice can shed light on shoot gravitropism and improvement of plant tiller/branch angle in other species, thereby contributing to agricultural production in the future.

Tiller angle is an important determinant of plant architecture in rice (Oryza sativa L.). Auxins play a critical role in determining plant architecture; however, the underlying metabolic and signaling mechanisms are still largely unknown. In this study, we have identified a member of the bZIP family of TGA class transcription factors, OsbZIP49, that participates in the regulation of plant architecture and is specifically expressed in gravity-sensing tissues, including the shoot base, nodes and lamina joints. Transgenic rice plants overexpressing OsbZIP49 displayed a tiller-spreading phenotype with reduced plant height and internode lengths. In contrast, CRISPR/Cas9-mediated knockout of OsbZIP49 resulted in a compact architecture. Follow-up studies indicated that the effects of OsbZIP49 on tiller angles are mediated through changes in shoot gravitropic responses. Additionally, we provide evidence that OsbZIP49 activates the expression of indole-3-acetic acid-amido synthetases OsGH3-2 and OsGH3-13 by directly binding to TGACG motifs located within the promoters of both genes. Increased GH3-catalyzed conjugation of indole-3-acetic acid (IAA) in rice transformants overexpressing OsbZIP49 resulted in the increased accumulation of IAA-Asp and IAA-Glu, and a reduction in local free auxin, tryptamine and IAA-Glc levels. Exogenous IAA or naphthylacetic acid (NAA) partially restored shoot gravitropic responses in OsbZIP49-overexpressing plants. Knockout of OsbZIP49 led to reduced expression of both OsGH3-2 and OsGH3-13 within the shoot base, and increased accumulation of IAA and increased OsIAA20 expression levels were observed in transformants following gravistimulation. Taken together, the present results reveal the role transcription factor OsbZIP49 plays in determining plant architecture, primarily due to its influence on local auxin homeostasis.

Rice (Oryza sativa) tiller angle is a key component for achieving ideal plant architecture and higher grain yield. However, the molecular mechanism underlying rice tiller angle remains elusive. We characterized a novel rice tiller angle mutant lazy2 (la2) and isolated the causative gene LA2 through map-based cloning. Biochemical, molecular and genetic studies were conducted to elucidate the LA2-involved tiller angle regulatory mechanism. The la2 mutant shows large tiller angle with impaired shoot gravitropism and defective asymmetric distribution of auxin. We found that starch granules in amyloplasts are completely lost in the gravity-sensing leaf sheath base cells of la2, whereas the seed development is not affected. LA2 encodes a novel chloroplastic protein that can interact with the starch biosynthetic enzyme Oryza sativa plastidic phosphoglucomutase (OspPGM) to regulate starch biosynthesis in rice shoot gravity-sensing cells. Genetic analysis showed that LA2 regulates shoot gravitropism and tiller angle by acting upstream of LA1 to mediate lateral auxin transport. Our studies revealed that LA2 acts as a novel regulator of rice tiller angle by specifically regulating starch biosynthesis in gravity-sensing cells, and established the framework of the starch-statolith-dependent rice tiller angle regulatory pathway, providing new insights into the rice tiller angle regulatory network.