Summary: Melatonin, a natural phytohormone in plants, plays multiple critical roles in plant growth and stress responses. Although melatonin biosynthesis‐related genes have been suggested to possess diverse biological functions, their roles and functional mechanisms in regulating rice grain yield remain largely unexplored. Here, we uncovered the roles of a caffeic acid O‐methyltransferase (OsCOMT) gene in mediating rice grain yield through dual regulation of leaf senescence and vascular development. In vitro and in vivo evidence revealed that OsCOMT is involved in melatonin biosynthesis. Transgenic assays suggested that OsCOMT significantly delays leaf senescence at the grain filling stage by inhibiting degradation of chlorophyll and chloroplast, which, in turn, improves photosynthesis efficiency. In addition, the number and size of vascular bundles in the culms and leaves were significantly increased in the OsCOMT‐overexpressing plants, while decreased in the knockout plants, suggesting that OsCOMT plays a positive role in vascular development of rice. Further evidence indicated that OsCOMT‐mediated vascular development might owe to the crosstalk between melatonin and cytokinin. More importantly, we found that OsCOMT is a positive regulator of grain yield, and overexpression of OsCOMT increase grain yield per plant even in a high‐yield variety background, suggesting that OsCOMT can be used as an important target for enhancing rice yield. Our findings shed novel insights into melatonin‐mediated leaf senescence and vascular development and provide a possible strategy for genetic improvement of rice grain yield.

Summary: Hybrid breeding has been shown to effectively increase rice productivity. However, identifying desirable hybrids out of numerous potential combinations is a daunting challenge. Genomic selection holds great promise for accelerating hybrid breeding by enabling early selection before phenotypes are measured. With the recent advances in multi‐omic technologies, hybrid prediction based on transcriptomic and metabolomic data has received increasing attention. However, the current omic‐based hybrid prediction has ignored parental phenotypic information, which is of fundamental importance in plant breeding. In this study, we integrated parental phenotypic information into various multi‐omic prediction models applied in hybrid breeding of rice and compared the predictabilities of 15 combinations from four sets of predictors from the parents, that is genome, transcriptome, metabolome and phenome. The predictability for each combination was evaluated using the best linear unbiased prediction and a modified fast HAT method. We found significant interactions between predictors and traits in predictability, but joint prediction with various combinations of the predictors significantly improved predictability relative to prediction of any single source omic data for each trait investigated. Incorporation of parental phenotypic data into various omic predictors increased the predictability, averagely by 13.6%, 54.5%, 19.9% and 8.3%, for grain yield, number of tillers per plant, number of grains per panicle and 1000 grain weight, respectively. Among nine models of incorporating parental traits, the AD‐All model was the most effective one. This novel strategy of incorporating parental phenotypic data into multi‐omic prediction is expected to improve hybrid breeding progress, especially with the development of high‐throughput phenotyping technologies.

Root system plays an essential role in water and nutrient acquisition in plants. Understanding the genetic basis of root development will be beneficial for breeding new cultivars with efficient root system to enhance resource use efficiency in maize. Here, the natural variation of 13 root and 3 shoot traits was evaluated in 297 maize inbred lines and genome-wide association mapping was conducted to identify SNPs associated with target traits. All measured traits exhibited 2.02- to 21.36-fold variations. A total of 34 quantitative trait loci (QTLs) were detected for 13 traits, and each individual QTL explained 5.7% to 15.9% of the phenotypic variance. Three pleiotropic QTLs involving five root traits were identified; SNP_2_104416607 was associated with lateral root length (LRL), root surface area (RA), root length between 0 and 0.5mm in diameter (RL005), and total root length (TRL); SNP_2_184016997 was associated with RV and RA, and SNP_4_168917747 was associated with LRL, RA and TRL. The expression levels of candidate genes in root QTLs were evaluated by RNA-seq among three long-root lines and three short-root lines. A total of five genes that showed differential expression between the long- and short-root lines were identified as promising candidate genes for the target traits. These QTLs and the potential candidate genes are important source data to understand root development and genetic improvement of root traits in maize.

The primary root is the first organ to perceive the stress signals for abiotic stress. In this study, maize plants subjected to drought, heat and combined stresses displayed a significantly reduced primary root length. Metabolic and transcriptional analyses detected 72 and 5,469 differentially expressed metabolites and genes in response to stress conditions, respectively. The functional annotation of differentially expressed metabolites and genes indicated that primary root development was mediated by pathways involving phenylalanine metabolism, hormone metabolism and signaling under stress conditions. Furthermore, we found that the concentration of salicylic acid and two precursors, shikimic acid and phenylalanine, showed rapid negative accumulation after all three stresses. The expression levels of some key genes involved in salicylic acid metabolism and signal transduction were differentially expressed under stress conditions. This study extends our understanding of the mechanism of primary root responses to abiotic stress tolerance in maize.

ZmPGP1, involved in the polar auxin transport, has been shown to be associated with plant height, leaf angle, yield traits, and root development in maize. To explore natural variation and domestication selection of ZmPGP1, we re-sequenced the ZmPGP1 gene in 349 inbred lines, 68 landraces, and 32 teosintes. Sequence polymorphisms, nucleotide diversity, and neutral tests revealed that ZmPGP1 might be selected during domestication and improvement processes. Marker–trait association analysis in inbred lines identified 11 variants significantly associated with 4 plant architecture and 5 ear traits. SNP1473 was the most significant variant for kernel length and ear grain weight. The frequency of an increased allele T was 40.6% in teosintes, and it was enriched to 60.3% and 89.1% during maize domestication and improvement. This result revealed that ZmPGP1 may be selected in the domestication and improvement process, and significant variants could be used to develop functional markers to improve plant architecture and ear traits in maize.

Lateral roots (LRs) branching is crucial for water and nutrient acquisition in plants, ultimately determining the overall plant performance and productivity. However, the transcriptional regulation of LR development in crops and its role in stress resilience remain largely unexplored. Leveraging integrated transcriptome-wide association study and single-cell RNA sequencing data, we identified a basic leucine zipper (bZIP) transcription factor ZmbZIP89 as an important regulator of LR elongation and mapped its spatial expression pattern in cortex/epidermis cell types. ZmbZIP89 can activate the expression of ZmPRX47 to regulate the production of root reactive oxygen species homeostasis, contributing to increased lateral root length (LRL) and enhanced drought resistance. Natural variations in the 3′ untranslated region of ZmbZIP89 enhance gene expression by increasing mRNA stability, leading to increases in LRL and drought tolerance. These findings contribute to our understanding of the molecular mechanisms underlying LR development and provide potential gene targets for breeding stress-resilient crops.