Brassinosteroid Signaling Pathway Research Articles

Exploration of ABA Responsive miRNAs Reveals a New Hormone Signaling Crosstalk Pathway Regulating Root Growth of Populus euphratica

Abscisic acid (ABA) plays an important role in the regulation of plant adaptation, seed germination, and root development in plants. However, the mechanism of ABA regulation of root development is still poorly understood, especially through the miRNA-mediated pathway. Here, small RNA (sRNA)-seq and degradome-seq were used to analyze the miRNAs’ responsive to ABA in the stems and roots of P. euphratica, a model tree species for abiotic stress-resistance research. In total, 255 unique mature sequences, containing 154 known miRNAs and 101 novel miRNAs were identified, among which 33 miRNAs and 54 miRNAs were responsive to ABA in the roots and stems, respectively. Furthermore, the analysis of these miRNAs and their targets revealed a new hormone signaling crosstalk model of ABA regulation of root growth through miRNA-mediated pathways, such as peu-miR-n68 mediation of the crosstalk between ABA and the brassinosteroid (BR) signaling pathway and peu-miR477b mediation of the crosstalk between ABA and Gibberellic acid (GA) signaling. Taken together, our genome-wide analysis of the miRNAs provides a new insight into the mechanism of ABA regulation of root growth in Populus.

Genome-wide transcriptomic analysis of BR-deficient Micro-Tom reveals correlations between drought stress tolerance and brassinosteroid signaling in tomato

Brassinosteroids (BRs) are plant steroid hormones that play crucial roles in a range of growth and developmental processes. Although BR signal transduction and biosynthetic pathways have been well characterized in model plants, their biological roles in an important crop, tomato (Solanum lycopersicum), remain unknown. Here, cultivated tomato (WT) and a BR synthesis mutant, Micro-Tom (MT), were compared using physiological and transcriptomic approaches. The cultivated tomato showed higher tolerance to drought and osmotic stresses than the MT tomato. However, BR-defective phenotypes of MT, including plant growth and stomatal closure defects, were completely recovered by application of exogenous BR or complementation with a SlDWARF gene. Using genome-wide transcriptome analysis, 619 significantly differentially expressed genes (DEGs) were identified between WT and MT plants. Several DEGs were linked to known signaling networks, including those related to biotic/abiotic stress responses, lignification, cell wall development, and hormone responses. Consistent with the higher susceptibility of MT to drought stress, several gene sets involved in responses to drought and osmotic stress were differentially regulated between the WT and MT tomato plants. Our data suggest that BR signaling pathways are involved in mediating the response to abiotic stress via fine-tuning of abiotic stress-related gene networks in tomato plants.

GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality

Identification of grain shape determining genes can facilitate breeding of rice cultivars with optimal grain shape and appearance quality. Here, we identify GS9 (Grain Shape Gene on Chromosome 9) gene by map-based cloning. The gs9 null mutant has slender grains, while overexpression GS9 results in round grains. GS9 encodes a protein without known conserved functional domain. It regulates grain shape by altering cell division. The interaction of GS9 and ovate family proteins OsOFP14 and OsOFP8 is modulated by OsGSK2 kinase, a key regulator of the brassinosteroids signaling pathway. Genetic interaction analysis reveals that GS9 functions independently from other previously identified grain size genes. Introducing the gs9 allele into elite rice cultivars significantly improves grain shape and appearance quality. It suggests potential application of gs9, alone or in combination with other grain size determining genes, in breeding of rice varieties with optimized grain shape.

Arabidopsis G-Protein β Subunit AGB1 Interacts with BES1 to Regulate Brassinosteroid Signaling and Cell Elongation.

In Arabidopsis, brassinosteroids (BR) are major growth-promoting hormones, which integrate with the heterotrimeric guanine nucleotide-binding protein (G-protein) signals and cooperatively modulate cell division and elongation. However, the mechanisms of interaction between BR and G-protein are not well understood. Here, we show that the G-protein β subunit AGB1 directly interacts with the BR transcription factor BES1 in vitro and in vivo. An AGB1-null mutant, agb1-2, displays BR hyposensitivity and brassinazole (BRZ, BR biosynthesis inhibitor) hypersensitivity, which suggests that AGB1 positively mediates the BR signaling pathway. Moreover, we demonstrate that AGB1 synergistically regulates expression of BES1 target genes, including the BR biosynthesis genes CPD and DWF4 and the SAUR family genes required for promoting cell elongation. Further, Western blot analysis of BES1 phosphorylation states indicates that the interaction between AGB1 and BES1 alters the phosphorylation status of BES1 and increases the ratio of dephosphorylated to phosphorylated BES1, which leads to accumulation of dephosphorylated BES1 in the nucleus. Finally, AGB1 promotes BES1 binding to BR target genes and stimulates the transcriptional activity of BES1. Taken together, our results demonstrate that AGB1 positively regulates cell elongation by affecting the phosphorylation status and transcriptional activity of BES1.

Crosstalk of brassinosteroids with other phytohormones under various abiotic stresses

Brassinosteroids (BRs) are the steroidal plant hormones that play crucial roles in both plant growth and progressions. In recent years advancements done in accessibility of biological possessions and approaches led to the better understanding of the various processes involved in BRs biosynthesis, transport, signaling and degradation pathways. The current researches are also associated to the flexible roles of BRs. From the previous studies it was evident that BRs interrelate with other phytohormones such as auxin, gibberellin, ethylene, cytokinin, abscisic acid, jasmonic acid, salicylic acid and polyamine in regulating various physiological and developmental processes in plants. In this section an effort is made to understand elusive development and growth directly or indirectly linked to BR homeostasis, signaling and its crosstalk with other phytohormones. This information will support emerging extrapolative representations to moderate various useful traits in plants and address current encounters in agriculture.

Abscisic Acid Signaling Inhibits Brassinosteroid Signaling through Dampening the Dephosphorylation of BIN2 by ABI1 and ABI2

Abscisic acid (ABA) and brassinosteroid (BR) antagonistically regulate many aspects of plant growth and development. Previous physiological studies have revealed that the inhibition of BR signaling by ABA is largely dependent on ABI1 and ABI2. However, the genetic and molecular basis of how ABI1 and ABI2 are involved in inhibiting BR signaling remains unclear. Although it is known that in the BR signaling pathway the ABA-BR crosstalk occurs in the downstream of BR receptor complex but upstream of BIN2 kinase, a negative regulator of BR signaling, the component that acts as the hub to directly mediate their crosstalk remains a big mystery. Here, we found that ABI1 and ABI2 interact with and dephosphorylate BIN2 to regulate its activity toward the phosphorylation of BES1. By in vitro mimicking ABA signal transduction, we found that ABA can promote BIN2 phosphorylation by inhibiting ABI2 through ABA receptors. RNA-sequencing analysis further demonstrated that ABA inhibits BR signaling through the ABA primary signaling components, including its receptors and ABI2, and that ABA and GSK3s co-regulate a common set of stress-responsive genes. Because BIN2 can interact with and phosphorylate SnRK2s to activate its kinase activity, our study also reveals there is a module of PP2Cs–BIN2–SnRK2s in the ABA signaling pathway. Collectively, these findings provide significant insights into how plants balance growth and survival by coordinately regulating the growth-promoting signaling pathway and stress responses under abiotic stresses.

Rice ERECT LEAF 1 acts in an alternative brassinosteroid signaling pathway independent of the receptor kinase OsBRI1

ABSTRACTERECT LEAF 1 (ELF1) was previously identified as a component of brassinosteroid signaling in rice. A double mutant obtained by crossing elf1-1 (a null mutant of ELF1) with d61-1 (a leaky mutant of OsBRI1) showed a more severe phenotype than did the elf1-1 single mutant, resembling that of a severe brassinosteroid-deficient mutant. Microarray analysis showed that the gene expression profile of elf1-1 was distinct from that of d61-12 (a leaky mutant of OsBRI1 with a phenotype similar to that of elf1-1), and fewer than half of genes differentially expressed between the wild-type and elf1-1 showed similar differences in d61-12 relative to the wild-type. These results indicate that less than half of ELF1-regulated genes in rice seedlings are affected by OsBRI1, and suggest that ELF1 acts in a rice brassinosteroid signaling pathway different from that initiated by OsBRI1. Gene expression analysis showed that some stress response-related genes were induced in elf1-1 but not in d61-12, and 8 of 9 genes oppositely regulated in elf1-1 and d61-12 were significantly up- or down-regulated in both elf1-1 and jasmonic acid-treated wild-type. These results imply that ELF1 suppresses stress-induced signalling, and that jasmonic acid signaling is stimulated in elf1-1; therefore, ELF1 may be involved in the brassinosteroid-mediated suppression of jasmonic acid response in rice.

Top Bending Panicle1 is involved in brassinosteroid signaling and regulates the plant architecture in rice

Brassinosteroids (BRs) regulate several aspects of plant growth and development. Although extensive studies have shown that BR signaling is conservative in higher plants, the molecular mechanism of regulating plant architecture in rice still remains to be explored. Here, we characterized a rice mutant named top bending panicle1 (tbp1). Compared to wild type, tbp1 mutant plants displayed semi-dwarf stature, erect leaves, small and round grains, as well as more tillers. Remarkably, the panicles of tbp1 plants were shorter and denser, and the tops of the panicles were curved by rolling of the base of flag leaves, which was later verified as due to reduced bulliform cell numbers. Map-based cloning, together with transgenic complementation and RNA-interference tests, revealed that TBP1 is a member of the somatic embryogenesis receptor kinases (SERKs) family involved in BR signaling. Furthermore, bimolecular fluorescence complementation and co-immunoprecipitation analysis demonstrated that a substitution at 61st amino acid (His61Leu) in the tbp1 mutant may result in a reduction of the interaction between TBP1 and OsBRI1 (BR receptor in rice). Taken together, our results demonstrate that TBP1 plays a significant role in regulating plant architecture via the brassinosteroid signaling pathway.

C4 Protein of Sweet Potato Leaf Curl Virus Regulates Brassinosteroid Signaling Pathway through Interaction with AtBIN2 and Affects Male Fertility in Arabidopsis.

Sweepoviruses have been identified globally and cause substantial yield losses and cultivar decline in sweet potato. This study aimed to investigate the interaction between sweepovirus and plant host by analyzing the function of the viral protein C4 of Sweet potato leaf curl virus-Jiangsu (SPLCV-JS), a sweepovirus cloned from diseased sweet potato plants in East China. Ectopic expression of the C4 in Arabidopsis altered plant development drastically with phenotypic changes including leaf curling, seedling twisting, deformation of floral tissues and reduction of pollen fertility, and seed number. Using bimolecular fluorescence complementation analysis, this study demonstrated that the SPLCV-JS C4 protein interacted with brassinosteroid-insensitive 2 (AtBIN2) in the plasma membrane of Nicotiana benthamiana cells. The C4 AtBIN2 interaction was further confirmed by yeast two-hybrid assays. This interaction led to the re-localization of AtBIN2-interacting proteins AtBES1/AtBZR1 into the nucleus which altered the expression of brassinosteroid (BR)-response genes, resulting in the activation of BR-signaling pathway. The interaction of SPLCV-JS C4 and AtBIN2 also led to the down-regulated expression of key genes involved in anther and pollen development, including SPROROCYTELESS/NOZZLE, DEFECTIVE IN TAPEL DEVELOPMENT AND FUNCTION 1, and ABORTED MICROSPORES, which caused abnormal tapetal development, followed by defective exine pattern formation of microspores and pollen release. Consequently, male fertility in the C4 transgenic Arabidopsis was reduced. The present study illustrated how the sweepovirus C4 protein functioned in host cells and affected male fertility by interacting with the key components of BR-signaling pathway.

SlBIR3 Negatively Regulates PAMP Responses and Cell Death in Tomato.

Bri1-associated kinase 1 (BAK1)-interacting receptor-like kinase (BIR) proteins have been shown to play important roles in regulating growth and development, pathogen associated molecular pattern (PAMP)-triggered immunity (PTI) responses, and cell death in the model plant, Arabidopsis thaliana. We identified four BIR family members in tomato (Solanum lycopersicum), including SlBIR3, an ortholog of AtBIR3 from A. thaliana. SlBIR3 is predicted to encode a membrane localized non-arginine-aspartate (non-RD) kinase that, based on protein sequence, does not have autophosphorylation activity but that can be phosphorylated in vivo. We established that SlBIR3 interacts with SlBAK1 and AtBAK1 using yeast two-hybrid assays and co-immunoprecipitation and maltose-binding protein pull down assays. We observed that SlBIR3 overexpression in tomato (cv. micro-tom) and A. thaliana has weak effect on growth and development through brassinosteroid (BR) signaling. SlBIR3 overexpression in A. thaliana suppressed flg22-induced defense responses, but did not affect infection with the bacterial pathogen Pseudomonas syringae (PstDC3000). This result was confirmed using virus-induced gene silencing (VIGS) in tomato in conjunction with PstDC3000 infection. Overexpression of SlBIR3 in tomato (cv. micro-tom) and A. thaliana resulted in enhanced susceptibility to the necrotrophic fungus Botrytis cinerea. In addition, co-silencing SlBIR3 with SlSERK3A or SlSERK3B using VIGS and the tobacco rattle virus (TRV)-RNA2 vector containing fragments of both the SlSERK3 and SlBIR3 genes induced spontaneous cell death, indicating a cooperation between the two proteins in this process. In conclusion, our study revealed that SlBIR3 is the ortholog of AtBIR3 and that it participates in BR, PTI, and cell death signaling pathways.

Overexpressed BRH1, a RING finger gene, alters rosette leaf shape in Arabidopsis thaliana.

Leaves are the most important plant parts for photosynthesis and respiration. Many genes are involved in determining leaf shape; however, little is known about the effects of brassinosteroid (BR) signaling-pathway genes on the development of leaf shape. Here, the brassinosteroid-responsive RING-H2 (BRH1) gene, which is suppressed by 24-epi-brassinolide treatment, was isolated from Arabidopsis thaliana. The amino acid sequence contained a highly conserved RING finger domain. In a phylogenetic analysis, BRH1 clustered closely with GLYMA11G02470.1. The leaves of brh1 mutant plants were not much different to those of the wild-type, while transgenic plants with high BRH1 expression levels had rounder rosette leaves. Mutants of the BR synthesis pathway also had a similar round leaf phenotype, and greater BRH1 expression levels. Moreover, the related marker genes KNAT1, AtHB13 and ROT4, which are known to control leaf shape, altered transcriptional levels in both transgenic BRH1 and BR-synthesis mutant lines. Thus, BRH1 may be involved in the BR signaling pathway and regulate the growth and development of rosette leaves. Research on BRH1 may prove valuable for understanding the regulatory mechanism of leaf shape and improving the leaf shapes of ornamental plants.

The role of brassinosteroids in the regulation of the plasma membrane H+-ATPase and NADPH oxidase under cadmium stress

The present research aim was to define the role of brassinosteroids (BRs) in plant adaptation to cadmium stress. We observed a stimulating effect of exogenous BR on the activity of two plasma membrane enzymes which play a key role in plants adaptation to cadmium stress, H+-ATPase (EC 3.6.3.14) and NADPH oxidase (EC 1.6.3.1). Using anti-phosphothreonine antibody we showed that modification of PM H+-ATPase activity under BR action could result from phosphorylation of the enzyme protein. Also the relative expression of genes encoding both PM H+-ATPase and NADPH oxidase was affected by BR. To confirm the role of BR in the cadmium stimulating effect on activity of both studied plasma membrane enzymes, an assay in the presence of a BR biosynthesis inhibitor (propiconazole) was performed. Moreover, as a tool in our work we used commercially available plant mutants unable to BR biosynthesis or with dysfunctional BR signaling pathway, to further confirm participation of BR in plant adaptation to heavy metal stress. Presented results demonstrate some elements of the brassinosteroid-induced pathway activated under cadmium stress, wherein H+-ATPase and NADPH oxidase are key factors.

Mathematical modelling and analysis of the brassinosteroid and gibberellin signalling pathways and their interactions

The plant hormones brassinosteroid (BR) and gibberellin (GA) have important roles in a wide range of processes involved in plant growth and development. In this paper we derive and analyse new mathematical models for the BR signalling pathway and for the crosstalk between the BR and GA signalling pathways. To analyse the effects of spatial heterogeneity of the signalling processes, along with spatially-homogeneous ODE models we derive coupled PDE-ODE systems modelling the temporal and spatial dynamics of molecules involved in the signalling pathways. The values of the parameters in the model for the BR signalling pathway are determined using experimental data on the gene expression of BR biosynthetic enzymes. The stability of steady state solutions of our mathematical model, shown for a wide range of parameters, can be related to the BR homeostasis which is essential for proper function of plant cells. Solutions of the mathematical model for the BR signalling pathway can exhibit oscillatory behaviour only for relatively large values of parameters associated with transcription factor brassinazole-resistant1’s (BZR) phosphorylation state, suggesting that this process may be important in governing the stability of signalling processes. Comparison between ODE and PDE-ODE models demonstrates distinct spatial distribution in the level of BR in the cell cytoplasm, however the spatial heterogeneity has significant effect on the dynamics of the averaged solutions only in the case when we have oscillations in solutions for at least one of the models, i.e. for possibly biologically not relevant parameter values. Our results for the crosstalk model suggest that the interaction between transcription factors BZR and DELLA exerts more influence on the dynamics of the signalling pathways than BZR-mediated biosynthesis of GA, suggesting that the interaction between transcription factors may constitute the principal mechanism of the crosstalk between the BR and GA signalling pathways. In general, perturbations in the GA signalling pathway have larger effects on the dynamics of components of the BR signalling pathway than perturbations in the BR signalling pathway on the dynamics of the GA pathway. The perturbation in the crosstalk mechanism also has a larger effect on the dynamics of the BR pathway than of the GA pathway. Large changes in the dynamics of the GA signalling processes can be observed only in the case where there are disturbances in both the BR signalling pathway and the crosstalk mechanism. Those results highlight the robustness of the GA signalling pathway.

Transcriptional Regulation of Brassinosteroid Accumulation during Carrot Development and the Potential Role of Brassinosteroids in Petiole Elongation.

It is widely known that brassinosteroids (BRs) are involved in various physiological processes during plant growth and development. Roles of BRs have been reported in many plants. However, relevant report is yet not found in carrot. Carrot is a nutrient-rich vegetable from the Apiaceae family. Here, we measured the bioactive contents of BRs at five successive stages and analyzed the expression profiles of genes involved in BR biosynthesis, signaling pathway and catabolism. We found that most biosynthesis regulated genes had higher expression level at the first development stage of carrot and the catabolism gene BAS1/CYP734A1 had significantly high expression level at the first stage in carrot roots and petioles. In addition, we treated carrot plants with exogenous 24-epibrassinolide (24-EBL) and examined the morphological changes after treating. Compared with control plants, carrot plants treated with 24-EBL had higher plant height, more number of petioles and heavier aboveground weight. The expression levels of DcBRI1, DcBZR1, and DcBSU1 in the petioles were significantly up-regulated by treating with exogenous 24-EBL. The expression profiles of DcCYP734A1 were all significantly up-regulated in the three organs when treated with 0.5 mg/L 24-EBL. The elongation of carrot petioles can be promoted by treating with exogenous 24-EBL. These results indicate that BRs playing potential roles during the growth and development of carrot.

Cross-talk of Brassinosteroid signaling in controlling growth and stress responses.

Plants are faced with a barrage of stresses in their environment and must constantly balance their growth and survival. As such, plants have evolved complex control systems that perceive and respond to external and internal stimuli in order to optimize these responses, many of which are mediated by signaling molecules such as phytohormones. One such class of molecules called Brassinosteroids (BRs) are an important group of plant steroid hormones involved in numerous aspects of plant life including growth, development and response to various stresses. The molecular determinants of the BR signaling pathway have been extensively defined, starting with the membrane-localized receptor BRI1 and co-receptor BAK1 and ultimately culminating in the activation of BES1/BZR1 family transcription factors, which direct a transcriptional network controlling the expression of thousands of genes enabling BRs to influence growth and stress programs. Here, we highlight recent progress in understanding the relationship between the BR pathway and plant stress responses and provide an integrated view of the mechanisms mediating cross-talk between BR and stress signaling.

BRS1 Function in Facilitating Lateral Root Emergence in Arabidopsis.

The BRS1 (BRI1 Suppressor 1) gene encodes a serine carboxypeptidase that plays a critical role in the brassinosteroid signaling pathway. However, its specific biological function remains unclear. In this study, the developmental role of BRS1 was investigated in Arabidopsis thaliana. We found that overexpressing BRS1 resulted in significantly more lateral roots in different Arabidopsis ecotypes (WS2 and Col-0) and in brassinosteroid mutants (bri1-5 and det2-28). Further research showed that BRS1 facilitates the process whereby lateral root primordia break through the endodermis, cortex, and epidermis. Consistent with this, BRS1 was found to be highly expressed in the root endodermis and accumulated in the extracellular space around the dome of the lateral root primordia. Taken together, these results highlight the role of BRS1 in the process of lateral root emergence and provide new insight into the role of serine carboxypeptidases in plant root development.

Multiple Ways of BES1/BZR1 Degradation to Decode Distinct Developmental and Environmental Cues in Plants

Plants must constantly integrate various environment stimuli and many endogenous hormones to optimize their growth and development. BRI1-EMS-SUPPRESSOR 1 (BES1) and BRASSINAZOLE RESISTANT 1 (BZR1) act not only as key transcription factors in the brassinosteroid (BR) signaling pathway, but also as a hub that integrates diverse signals to regulate plant development and environment adaptability (Wang et al., 2014). Both BES1 and BZR1 were identified through forward genetic screens of mutants with constitutively activated BR signaling.

Scanning for New BRI1 Mutations via TILLING Analysis.

The identification and characterization of a mutational spectrum for a specific protein can help to elucidate its detailed cellular functions. BRASSINOSTEROID INSENSITIVE1 (BRI1), a multidomain transmembrane receptor-like kinase, is a major receptor of brassinosteroids in Arabidopsis (Arabidopsis thaliana). Within the last two decades, over 20 different bri1 mutant alleles have been identified, which helped to determine the significance of each domain within BRI1. To further understand the molecular mechanisms of BRI1, we tried to identify additional alleles via targeted induced local lesions in genomes. Here, we report our identification of 83 new point mutations in BRI1, including nine mutations that exhibit an allelic series of typical bri1 phenotypes, from subtle to severe morphological alterations. We carried out biochemical analyses to investigate possible mechanisms of these mutations in affecting brassinosteroid signaling. A number of interesting mutations have been isolated via this study. For example, bri1-702, the only weak allele identified so far with a mutation in the activation loop, showed reduced autophosphorylation activity. bri1-705, a subtle allele with a mutation in the extracellular portion, disrupts the interaction of BRI1 with its ligand brassinolide and coreceptor BRI1-ASSOCIATED RECEPTOR KINASE1. bri1-706, with a mutation in the extracellular portion, is a subtle defective mutant. Surprisingly, root inhibition analysis indicated that it is largely insensitive to exogenous brassinolide treatment. In this study, we found that bri1-301 possesses kinase activity in vivo, clarifying a previous report arguing that kinase activity may not be necessary for the function of BRI1. These data provide additional insights into our understanding of the early events in the brassinosteroid signaling pathway.

Light involved regulation of BZR1 stability and phosphorylation status to coordinate plant growth in Arabidopsis.

Light and brassinosteroid (BR) are master environmental stimulus and endogenous cue for plant growth and development respectively. Great progress has been made in elucidating the molecular mechanisms on the cross-talk between light and BR. However, little is known about how BZR1, the pivotal integration node, is regulated by light and dark. Here, we demonstrated that an intact BR signaling pathway is essential for dark-induced hypocotyl elongation. Consequent expression assay showed that light–dark switch affected BZR1 phosphorylation and accumulation. Moreover, blocking the 26S proteasome pathway promoted the accumulation of both phosphorylated and dephosphorylated BZR1 proteins. Restriction of new protein biosynthesis had multiple effects on BZR1 phosphorylation status and stability, relying on the availability of light and the 26S proteasome pathways. Furthermore, sugar treatment strikingly enhanced the accumulation of total BZR1 under either light or dark conditions, likely by repressing transcript abundance of MAX2, a gene encoding an E3 ligase for BZR1. Finally, light-regulated phosphorylation change of BZR1 requires the existence of endogenous BR as well as functional BIN2 and protein phosphatase 2A (PP2A). Taken together, our results depicted a light-involved complex regulation network of BZR1 stability and phosphorylation status.

Crop Seed Size: BR Matters

Sufficient food supply is critically important to humans, and food security will be particularly challenging in view of the ever-growing world population, decreasing arable cropland, and global warming. To meet the challenges, most crop geneticists think it will be necessary to enrich the cultivated gene pool for breeding programs, and thus equally important to increase our understanding of the underlying genetic and molecular mechanism for grain yield. However, crop yield is a complex trait that is controlled simultaneously by multiple genes (i.e., quantitative trait loci [QTLs]) and heavily influenced by the surrounding environment; hence, to dissect such a complex trait into component contributory traits is necessary.