Climate change poses daunting challenges to agricultural production and food security. Rising temperatures, shifting weather patterns, and more frequent extreme events have already demonstrated their effects on local, regional, and global agricultural systems. Crop varieties that withstand climate-related stresses and are suitable for cultivation in innovative cropping systems will be crucial to maximize risk avoidance, productivity, and profitability under climate-changed environments. We surveyed 588 expert stakeholders to predict current and novel traits that may be essential for future pearl millet, sorghum, maize, groundnut, cowpea, and common bean varieties, particularly in sub-Saharan Africa. We then review the current progress and prospects for breeding three prioritized future-essential traits for each of these crops. Experts predict that most current breeding priorities will remain important, but that rates of genetic gain must increase to keep pace with climate challenges and consumer demands. Importantly, the predicted future-essential traits include innovative breeding targets that must also be prioritized; for example, 1) optimized rhizosphere microbiome, with benefits for P, N, and water use efficiency, 2) optimized performance across or in specific cropping systems, 3) lower nighttime respiration, 4) improved stover quality, and 5) increased early vigor. We describe cutting-edge tools and approaches to discover, validate, and incorporate novel genetic diversity from exotic germplasm into breeding populations with unprecedented precision, accuracy, and speed, concluding that the greatest challenge to developing crop varieties to win the race between climate change and food security might be our innovativeness in defining and boldness to breed for the traits of tomorrow.

Crop yield plays a critical role in global food security. For optimal plant growth and maximizing crop yield, nutrients must be balanced. However, the potential significance of balanced nitrogen-iron (N-Fe) for improving crop yield and nitrogen use efficiency (NUE) has never been addressed. Here, we show that balanced N-Fe sufficiency significantly increases tiller number and boosts yield and NUE in rice and wheat. NIN-like protein 4 (OsNLP4) plays a pivotal role in maintaining the N-Fe balance by coordinately regulating the expression of multiple genes in N and Fe metabolism and signaling. Moreover, OsNLP4 suppresses OsD3 expression and strigolactone (SL) signaling, thereby promoting tillering. Balanced N-Fe sufficiency promotes OsNLP4 nuclear localization by reducing H2O2, reinforcing all the functions of OsNLP4. Interestingly, OsNLP4 upregulates a set of H2O2-scavenging genes, thus promoting its own levels in the nucleus. We demonstrate that foliar spraying of balanced N-Fe fertilizer at the tillering stage can effectively increase tillers, yield and NUE of both rice and wheat in the field. Our findings reveal the previously unrecognized tremendous impacts of N-Fe balance on yield and NUE and the molecular mechanism by which the OsNLP4-OsD3 module integrates N-Fe nutrient signals to downregulate SL signaling and thereby promote rice tillering, shedding light on how N-Fe nutrient signals modulate tillering and providing guidelines for innovative fertilization to promote yield with reduced N fertilizer input, thus benefitting sustainable agriculture worldwide.

The RIPENING-INHIBITOR (RIN) transcriptional factor is a key regulator governing fruit ripening. While RIN also affects other physiological processes, its potential roles in triggering interactions with the rhizosphere microbiome and plant health are unknown. Here we show that RIN affects microbiome-mediated disease resistance via root exudation, leading to recruitment of microbiota that suppress the soil-borne, phytopathogenic Ralstonia solanacearum bacterium. Compared with the wild-type (WT) plant, RIN mutants had different root exudate profiles, which were associated with distinct changes in microbiome composition and diversity. Specifically, the relative abundances of antibiosis-associated genes and pathogen-suppressing Actinobacteria (Streptomyces) were clearly lower in the rhizosphere of rin mutants. The composition, diversity, and suppressiveness of rin plant microbiomes could be restored by the application of 3-hydroxyflavone and riboflavin, which were exuded in much lower concentrations by the rin mutant. Interestingly, RIN-mediated effects on root exudates, Actinobacteria, and disease suppression were evident from the seedling stage, indicating that RIN plays a dual role in the early assembly of disease-suppressive microbiota and late fruit development. Collectively, our work suggests that, while plant disease resistance is a complex trait driven by interactions between the plant, rhizosphere microbiome, and the pathogen, it can be indirectly manipulated using "prebiotic" compounds that promote the recruitment of disease-suppressive microbiota.

Plant architecture and panicle architecture are two critical agronomic traits that greatly affect the yield of rice (Oryza sativa). PROSTRATE GROWTH 1 (PROG1) encodes a key C2H2-type zinc-finger transcription factor and has pleiotropic effects on the regulation of both plant and panicle architecture, thereby influencing the grain yield. However, the molecular mechanisms through which PROG1 controls plant and panicle architecture remain unclear. In this study, we showed that PROG1 directly binds the LAZY 1 (LA1) promoter and acts as a repressor to inhibit LA1 expression. Conversely, LA1 acts as a repressor of PROG1 by directly binding to the PROG1 promoter. These two genes play antagonistic roles in shaping plant architecture by regulating both tiller angle and tiller number. Interestingly, our data showed that PROG1 controls panicle architecture through direct binding to the intragenic regulatory regions of OsGIGANTEA (OsGI) and subsequent activation of its expression. Collectively, we have identified two crucial targets of PROG1, LA1 and OsGI, shedding light on the molecular mechanisms underlying plant and panicle architecture control by PROG1. Our study provides valuable insights into the regulation of key domestication-related traits in rice and identifies potential targets for future high-yield rice breeding.

Wheat (Triticum aestivum L.) is a staple food for about 40% of the world's population. As the global population growth and living standards improvement, high yield and improved nutritional quality have become the main targets for wheat breeding. However, wheat production has been compromised by global warming through the more frequent occurrence of extreme temperature events, which increased water scarcity, aggravated soil salinization, and caused the plants more vulnerable to diseases, and can directly reduce plant fertility and suppress yield. One promising option to address these challenges is the genetic improvement of wheat for enhanced resistance to environmental stress. Several decades of progress in genomics and genetic engineering has tremendously advanced our understanding of the molecular and genetic mechanisms underlying abiotic and biotic stress responses in wheat. These advances have heralded what might be considered a "golden age" of functional genomics for the genetic improvement of wheat. Here, we summarize the current knowledge on the molecular and genetic basis of wheat resistance to abiotic and biotic stresses: the QTL/genes involved, their functional and regulatory mechanisms, and related strategies for genetic modification of wheat for improved stress resistance. In addition, we also provide perspectives on some key challenges that need to be addressed.

Nodulation is an energy-expensive behavior driven by legumes by providing carbon sources to bacteroids and obtaining nitrogen sources in return. The energy sensor sucrose nonfermenting 1-related protein kinase 1 (SnRK1) is the hub of energy regulation in eukaryotes. However, the molecular mechanism by which SnRK1 coordinates the allocation of energy and substances during symbiotic nitrogen fixation (SNF) remains unknown. In this study, we identified the novel legume-specific SnRK1α4, a member of the SnRK1 family that positively regulates SNF. Phenotypic analysis showed that nodule size and nitrogenase activity increased in SnRK1α4-overexpressing plants and decreased significantly in snrk1α4 mutants. We demonstrated that a key upstream kinase involved in nodulation, Does Not Make Infection 2 (DMI2), can phosphorylate SnRK1α4 at Thr175 to cause its activation. Further evidence clarified that SnRK1α4 phosphorylates the malate dehydrogenases MDH1/2 to promote malate production in the cytoplasm, supplying carbon sources to bacteroids. Therefore, our findings reveal an essential role of the DMI2-SnRK1α4-MDH pathway in supplying carbon sources to bacteroids for SNF and provide a new module for constructing cereal crops with SNF.

The shoot meristem generates the entire shoot system and is precisely maintained throughout the life cycle under various environmental challenges. In this study, we identified a prion-like domain (PrD) in the key shoot meristem regulator SHOOT MERISTEMLESS (STM), which distinguishes STM from other related KNOX1 proteins. We demonstrated that PrD stimulates STM to form nuclear condensates, which are required for maintaining the shoot meristem. STM nuclear condensate formation is stabilized by selected PrD-containing STM-interacting BELL proteins in vitro and in vivo. Moreover, condensation of STM promotes its interaction with the Mediator complex subunit MED8 and thereby enhances its transcriptional activity. Thus, condensate formation emerges as a novel regulatory mechanism of shoot meristem functions. Furthermore, we found that the formation of STM condensates is enhanced upon salt stress, which allows enhanced salt tolerance and increased shoot branching. Our findings highlight that the transcription factor partitioning plays an important role in cell fate determination and might also act as a tunable environmental acclimation mechanism.

Common buckwheat (Fagopyrum esculentum) is an ancient crop with a world-wide distribution. Due to its excellent nutritional quality and high economic and ecological value, common buckwheat is becoming increasingly important throughout the world. The availability of a high-quality reference genome sequence and population genomic data will accelerate the breeding of common buckwheat, but the high heterozygosity due to the outcrossing nature has greatly hindered the genome assembly. Here we report the assembly of a chromosome-scale high-quality reference genome of F. esculentum var. homotropicum, a homozygous self-pollinating variant of common buckwheat. Comparative genomics revealed that two cultivated buckwheat species, common buckwheat (F. esculentum) and Tartary buckwheat (F. tataricum), underwent metabolomic divergence and ecotype differentiation. The expansion of several gene families in common buckwheat, including FhFAR genes, is associated with its wider distribution than Tartary buckwheat. Copy number variation of genes involved in the metabolism of flavonoids is associated with the difference of rutin content between common and Tartary buckwheat. Furthermore, we present a comprehensive atlas of genomic variation based on whole-genome resequencing of 572 accessions of common buckwheat. Population and evolutionary genomics reveal genetic variation associated with environmental adaptability and floral development between Chinese and non-Chinese cultivated groups. Genome-wide association analyses of multi-year agronomic traits with the content of flavonoids revealed that Fh05G014970 is a potential major regulator of flowering period, a key agronomic trait controlling the yield of outcrossing crops, and that Fh06G015130 is a crucial gene underlying flavor-associated flavonoids. Intriguingly, we found that the gene translocation and sequence variation of FhS-ELF3 contribute to the homomorphic self-compatibility of common buckwheat. Collectively, our results elucidate the genetic basis of speciation, ecological adaptation, fertility, and unique flavor of common buckwheat, and provide new resources for future genomics-assisted breeding of this economically important crop.

Improving grain quality is a primary objective in contemporary rice breeding. Japanese modern rice breeding has developed two different types of rice, eating and sake-brewing rice, with different grain characteristics, indicating the selection of variant gene alleles during the breeding process. Given the critical importance of promptly and efficiently identifying genes selected in past breeding for future molecular breeding, we conducted genome scans for divergence, genome-wide association studies, and map-based cloning. Consequently, we successfully identified two genes, OsMnS and OsWOX9D, both contributing to rice grain traits. OsMnS encodes a mannan synthase that increases the white core frequency in the endosperm, a desirable trait for sake brewing but decreases the grain appearance quality. OsWOX9D encodes a grass-specific homeobox-containing transcription factor, which enhances grain width for better sake brewing. Furthermore, haplotype analysis revealed that their defective alleles were selected in East Asia, but not Europe, during modern improvement. In addition, our analyses indicate that a reduction in grain mannan content during African rice domestication may also be caused a defective OsMnS allele due to breeding selection. This study not only reveals the delicate balance between grain appearance quality and nutrition in rice but also provides a new strategy for isolating causal genes underlying complex traits, based on the concept of "breeding-assisted genomics" in plants.

Photosynthesis in both crops and natural vegetation allows light energy to be converted into chemical energy, and thus forms the foundation for almost all terrestrial trophic networks on Earth. The efficiency of photosynthetic energy conversion plays a crucial role in determining the portion of incident solar radiation that can be used to generate plant biomass throughout a growth season. Consequently, alongside factors such as resource availability, crop management, crop selection, maintenance costs, and intrinsic yield potential, photosynthetic energy use efficiency significantly influences crop yield. Photosynthetic efficiency is relevant to sustainability and food security because it impacts water-use efficiency, nutrient-use efficiency, and land-use efficiency. This review focuses specifically on the potential for improvements in photosynthetic efficiency to drive a sustainable increase in crop yields. We will discuss bypassing photorespiration, enhancing light use efficiency, harnessing natural variation in photosynthetic parameters for breeding purposes, and adopting new-to-nature approaches that show promise for achieving unprecedented gains in photosynthetic efficiency.