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.

Terrestrial plants can affect the growth and health of adjacent plants via interspecific interaction. Here, we studied the mechanism by which plant root exudates affect the recruitment of the rhizosphere microbiome in adjacent plants-with implications for plant protection-using a tomato (Solanum lycopersicum)-potatoonion (Allium cepa var. agrogatum) intercropping system. First, we showed that the intercropping system results in a disease-suppressive rhizosphere microbiome that protects tomato plants against Verticillium wilt disease caused by the soilborne pathogen Verticillium dahliae. Second, 16S rRNA gene sequencing revealed that intercropping with potatoonion altered the composition of the tomato rhizosphere microbiome by promoting the colonization of specific Bacillus sp. This taxon was isolated and shown to inhibit V. dahliae growth and induce systemic resistance in tomato plants. Third, a belowground segregation experiment found that root exudates mediated the interspecific interaction between potatoonion and tomato. Moreover, experiments using split-root tomato plants found that root exudates from potatoonion, especially taxifolin-a flavonoid compound-stimulate tomato plants to recruit plant-beneficial bacteria, such as Bacillus sp. Lastly, ultra-high-pressure liquid chromatography-mass spectrometry analysis found that taxifolin alters tomato root exudate chemistry; thus, this compound acts indirectly in modulating root colonization by Bacillus sp. Our results revealed that this intercropping system can improve tomato plant fitness by changing rhizosphere microbiome recruitment via the use of signaling chemicals released by root exudates of potatoonion. This study revealed a novel mechanism by which interspecific plant interaction modulates the establishment of a disease-suppressive microbiome, thus opening up new avenues of research for precision plant microbiome manipulations.

Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) are required for host defense against pathogens. Although PTI and ETI are intimately connected, the underlying molecular mechanisms remain elusive. In this study, we demonstrate that flg22 priming attenuates Pseudomonas syringae pv. tomato DC3000 (Pst) AvrRpt2-induced hypersensitive cell death, resistance, and biomass reduction in Arabidopsis. Mitogen-activated protein kinases (MAPKs) are key signaling regulators of PTI and ETI. The absence of MPK3 and MPK6 significantly reduces pre-PTI-mediated ETI suppression (PES). We found that MPK3/MPK6 interact with and phosphorylate the downstream transcription factor WRKY18, which regulates the expression of AP2C1 and PP2C5, two genes encoding protein phosphatases. Furthermore, we observed that the PTI-suppressed ETI-triggered cell death, MAPK activation, and growth retardation are significantly attenuated in wrky18/40/60 and ap2c1 pp2c5 mutants. Taken together, our results suggest that the MPK3/MPK6-WRKYs-PP2Cs module underlies PES and is essential for the maintenance of plant fitness during ETI.

The secondary vascular tissue emanating from meristems is central to understanding how vascular plants such as forest trees evolve, grow, and regulate secondary radial growth. However, the overall molecular characterization of meristem origins and developmental trajectories from primary to secondary vascular tissues in woody tree stems is technically challenging. In this study, we combined high-resolution anatomic analysis with a spatial transcriptome (ST) technique to define features of meristematic cells in a developmental gradient from primary to secondary vascular tissues in poplar stems. The tissue-specific gene expression of meristems and derived vascular tissue types were accordingly mapped to specific anatomical domains. Pseudotime analyses were used to track the origins and changes of meristems throughout the development from primary to secondary vascular tissues. Surprisingly, two types of meristematic-like cell pools within secondary vascular tissues were inferred based on high-resolution microscopy combined with ST, and the results were confirmed by in situ hybridization of, transgenic trees, and single-cell sequencing. The rectangle shape procambium-like (PCL) cells develop from procambium meristematic cells and are located within the phloem domain to produce phloem cells, whereas fusiform shape cambium zone (CZ) meristematic cells develop from fusiform metacambium meristematic cells and are located inside the CZ to produce xylem cells. The gene expression atlas and transcriptional networks spanning the primary transition to secondary vascular tissues generated in this work provide new resources for studying the regulation of meristem activities and the evolution of vascular plants. A web server (https://pgx.zju.edu.cn/stRNAPal/) was also established to facilitate the use of ST RNA-seq data.

Nuclear proteins are major constituents and key regulators of nucleome topological organization and manipulators of nuclear events. To decipher the global connectivity of nuclear proteins and the hierarchically organized modules of their interactions, we conducted two rounds of cross-linking mass spectrometry (XL-MS) analysis, one of which followed a quantitative double chemical cross-linking mass spectrometry (in vivoqXL-MS) workflow, and identified 24,140 unique crosslinks in total from the nuclei of soybean seedlings. This in vivo quantitative interactomics enabled the identification of 5340 crosslinks that can be converted into 1297 nuclear protein-protein interactions (PPIs), 1220 (94%) of which were non-confirmative (or novel) nuclear PPIs compared with those in repositories. There were 250 and 26 novel interactors of histones and the nucleolar box C/D small nucleolar ribonucleoprotein complex, respectively. Modulomic analysis of orthologous Arabidopsis PPIs produced 27 and 24 master nuclear PPI modules (NPIMs) that contain the condensate-forming protein(s) and the intrinsically disordered region-containing proteins, respectively. These NPIMs successfully captured previously reported nuclear protein complexes and nuclear bodies in the nucleus. Surprisingly, these NPIMs were hierarchically assorted into four higher-order communities in a nucleomic graph, including genome and nucleolus communities. This combinatorial pipeline of 4C quantitative interactomics and PPI network modularization revealed 17 ethylene-specific module variants that participate in a broad range of nuclear events. The pipeline was able to capture both nuclear protein complexes and nuclear bodies, construct the topological architectures of PPI modules and module variants in the nucleome, and probably map the protein compositions of biomolecular condensates.

Multiple enzymes perform moonlighting functions distinct from their main roles. UDP-glucose epimerases (UGEs), a subclass of isomerases, catalyze the interconversion of UDP-glucose (UDP-Glc) and UDP-galactose (UDP-Gal). We identified a rice male-sterile mutant, osuge1, with delayed tapetum degradation and abortive pollen. The mutant osuge1 protein lacked UDP-glucose epimerase activity, resulting in higher UDP-Gal content and lower UDP-Glc levels in the osuge1 mutant compared with the wild type. Interestingly, we discovered that OsUGE1 participates in the TIP2/bHLH142-TDR-EAT1/DTD transcriptional regulatory cascade involved in tapetum degradation, in which TIP2 and TDR regulate the expression of OsUGE1 while OsUGE1 regulates the expression of EAT1. In addition, we found that OsUGE1 regulates the expression of its own gene by directly binding to an E-box element in the OsUGE1 promoter. Collectively, our results indicate that OsUGE1 not only functions as a UDP-glucose epimerase but also moonlights as a transcriptional activator to promote tapetum degradation, revealing a novel regulatory mechanism of rice reproductive development.

N6-methyladenosine (m6A), which is added, removed, and interpreted by m6A writers, erasers, and readers, respectively, is the most abundant modification in eukaryotic mRNAs. The m6A marks play a pivotal role in the regulation of floral transition in plants. FLOWERING LOCUS K (FLK), an RNA-binding protein harboring K-homology (KH) motifs, is known to regulate floral transition by repressing the levels of a key floral repressor FLOWERING LOCUS C (FLC) in Arabidopsis. However, the molecular mechanism underlying FLK-mediated FLC regulation remains unclear. In this study, we identified FLK as a novel mRNA m6A reader protein that directly binds the m6A site in the 3'-untranslated region of FLC transcripts to repressing FLC levels by reducing its stability and splicing. Importantly, FLK binding of FLC transcripts was abolished in vir-1, an m6A writer mutant, and the late-flowering phenotype of the flk mutant could not be rescued by genetic complementation using the mutant FLKm gene, in which the m6A reader encoding function was eliminated, indicating that FLK binds and regulates FLC expression in an m6A-dependent manner. Collectively, our study has addressed a long-standing question of how FLK regulates FLC transcript levels and established a molecular link between the FLK-mediated recognition of m6A modifications on FLC transcripts and floral transition in Arabidopsis.

Most organisms adjust their development according to the environmental conditions. For the majority, this implies the sensing of alterations to cell walls caused by different cues. Despite the relevance of this process, few molecular players involved in cell wall sensing are known and characterized. Here, we show that the wall-associated kinase-like protein RESISTANCE TO FUSARIUM OXYSPORUM 1 (RFO1) is required for plant growth and early defense against Fusarium oxysporum and functions by sensing changes in the pectin methylation levels in the cell wall. The RFO1 dwell time at the plasma membrane is affected by the pectin methylation status at the cell wall, regulating MITOGEN-ACTIVATED PROTEIN KINASE and gene expression. We show that the extracellular domain of RFO1 binds de-methylated pectin in vitro, whose distribution in the cell wall is altered during F. oxysporum infection. Further analyses also indicate that RFO1 is required for the BR-dependent plant growth alteration in response to inhibition of pectin de-methyl-esterase activity at the cell wall. Collectively, our work demonstrates that RFO1 is a sensor of the pectin methylation status that plays a unique dual role in plant growth and defense against vascular pathogens.

Modern semi-dwarf rice varieties of the "Green Revolution" require a high supply of nitrogen (N) fertilizer to produce high yields. A better understanding of the interplay between N metabolism and plant developmental processes is required for improved N-use efficiency and agricultural sustainability. Here, we show that strigolactones (SLs) modulate root metabolic and developmental adaptations to low N availability for ensuring efficient uptake and translocation of available N. The key repressor DWARF 53 (D53) of the SL signaling pathway interacts with the transcription factor GROWTH-REGULATING FACTOR 4 (GRF4) and prevents GRF4 from binding to its target gene promoters. N limitation induces the accumulation of SLs, which in turn promotes SL-mediated degradation of D53, leading to the release of GRF4 and thus promoting the expression of genes associated with N metabolism. N limitation also induces degradation of the DELLA protein SLENDER RICE 1 (SLR1) in an D14- and D53-dependent manner, effectively releasing GRF4 from competitive inhibition caused by SLR1. Collectively, our findings reveal a previously unrecognized mechanism underlying SL and gibberellin crosstalk in response to N availability, advancing our understanding of plant growth-metabolic coordination and facilitating the design of the strategies for improving N-use efficiency in high-yield crops.

Pear is an important fruit tree that is widely distributed around the world. The first pear genome map was reported from our laboratory approximately 10 years ago. To further study global protein expression patterns in pear, we generated pear proteome data based on 24 major tissues. The tissue-resolved profiles provided evidence of the expression of 17 953 proteins. We identified 4294 new coding events and improved the pear genome annotation via the proteogenomic strategy based on 18 090 peptide spectra with peptide spectrum matches >1. Among the eight randomly selected new short coding open reading frames that were expressed in the style, four promoted and one inhibited the growth of pear pollen tubes. Based on gene coexpression module analysis, we explored the key genes associated with important agronomic traits, such as stone cell formation in fruits. The network regulating the synthesis of lignin, a major component of stone cells, was reconstructed, and receptor-like kinases were implicated as core factors in this regulatory network. Moreover, we constructed the online database PearEXP (http://www.peardb.org.cn) to enable access to the pear proteogenomic resources. This study provides a paradigm for in-depth proteogenomic studies of woody plants.

RNA quality control nonsense-mediated decay is involved in viral restriction in both plants and animals. However, it is not known whether two other RNA quality control pathways, nonstop decay and no-go decay, are capable of restricting viruses in plants. Here, we show that the evolutionarily conserved Pelota-Hbs1 complex negatively regulates infection of plant viruses in the family Potyviridae (termed potyvirids), the largest group of plant RNA viruses that accounts for more than half of the viral crop damage worldwide. Pelota enables the recognition of the functional G1-2A6-7 motif in the P3 cistron, which is conserved in almost all potyvirids. This allows Pelota to target the virus and act as a viral restriction factor. Furthermore, Pelota interacts with the SUMO E2-conjugating enzyme SCE1 and is SUMOylated in planta. Blocking Pelota SUMOylation disrupts the ability to recruit Hbs1 and inhibits viral RNA degradation. These findings reveal the functional importance of Pelota SUMOylation during the infection of potyvirids in plants.