Root-knot nematodes establish long-term parasitic relationships with diverse hosts by inducing specialized feeding cells. However, the molecular mechanisms by which nematodes manipulate this developmental reprogramming process remain largely unknown. Here we identify a class of ROOT MERISTEM GROWTH FACTOR (RGF)-like peptide effectors conserved in root-knot nematodes. MgRGF from Meloidogyne graminicola and MiRGF1 from M. incognita are expressed in subventral gland cells during early infection and secreted into the host apoplast. Functional analysis reveals that nematode RGFs are critical for feeding site development. Intriguingly, these peptides elicit host-specific outcomes in Arabidopsis and rice, involving both cell proliferation and expansion-two processes essential for establishing feeding cell identity. Further genetic and biochemical evidence demonstrates that nematode RGF peptides functionally mimic plant endogenous RGFs by hijacking the host RGI-receptor-mediated signalling pathway to regulate root growth and promote parasitism. Beyond PLT transcription factors, PSY peptide genes were identified as key downstream components of this RGF signalling cascade in rice. Functional characterization of OsPSY5 suggests its positive role in promoting cell elongation and facilitating nematode parasitism. Our findings unveil a cross-kingdom mimicry strategy whereby root-knot nematode-secreted RGF peptides co-opt host RGF signalling to orchestrate feeding cell formation, highlighting potential targets for engineering nematode resistance in crops.
Low bioavailability of inorganic phosphate (Pi) in soil severely constrains plant growth and crop productivity. Here, we demonstrate that Pi deficiency induced localised lignification in rice roots. Overexpression of OsDIR55, a beneficial gene we previously implicated in salt tolerance, significantly enhances plant performance under low Pi conditions, characterised by increased root-to-shoot ratio and biomass accumulation, whereas loss-of-function dir55 mutants exhibit contrast phenotypes. Importantly, the transcription factor OsPHR2 physically binds to the P1BS cis-elements in the OsDIR55 promoter, and Pi deprivation upregulates OsDIR55 expression in an OsPHR2-dependent manner. We further showed that OsDIR55 maintains cellular Pi homoeostasis under Pi starvation by reinforcing root apoplastic barrier functionality. Disruption of OsDIR55 leads to excessive Pi accumulation and aberrant physiological responses under Pi-sufficient conditions with leaf tip necrosis, indicative of Pi toxicity. Our work uncovers an essential role of the OsPHR2-OsDIR55 module in mediating root anatomical adaptations to Pi scarcity, refines Pi stress signalling pathways and highlights the significance of lignification in plant responses to environmental stresses.
Leaf senescence is a tightly regulated developmental process orchestrated by multiple transcription factor (TF) families. Although C2H2-type zinc finger proteins are known to participate in various aspects of plant growth and abiotic stress responses, their specific role in regulating leaf senescence remains poorly understood. Here, we show that knockout mutation of the C2H2-type zinc finger TF gene ZOS202 (LOC_Os02g02424) resulted in delayed leaf senescence under both dark-induced and natural conditions, while overexpression lines exhibit accelerated leaf senescence, as indicated by reactive oxygen species (ROS) overaccumulation, chloroplast degradation, and leaf cell death. As a dual-function transcription factor whose expression peaks at senescence onset, ZOS202 directly activates senescence-associated TF genes OsWRKY42, OsWRKY53, and ONAC096, while repressing peroxidase genes OsPRX113, OsPRX114, and OsPRX122, thereby disrupting ROS homeostasis and promoting senescence. Collectively, our findings uncover ZOS202 as a positive regulator of leaf senescence that acts by coordinating chlorophyll breakdown and ROS accumulation, providing promising strategies for fine-tuning leaf senescence in rice breeding.
Nitrogen (N) and phosphorus (P) are indispensable macronutrients for crop growth and productivity; however, their excessive application in agriculture has caused severe environmental degradation. Enhancing crop N-use efficiency (NUE) and P-use efficiency (PUE) is a critical strategy to reconcile high productivity with sustainability. In this review, we systematically synthesize recent advances in the genetic basis of NUE and PUE in crops, focusing on key traits and their associated signaling networks. We summarize the identification of N/P-efficiency genes and explore how natural variations in these genes correlate with soil nutrient availability, revealing adaptive patterns from crop domestication. Given the distinct biogeochemical behaviors of N and P, we propose tailored strategies that leverage nutrient-specific traits to optimize environment-resource coordination and yield-quality balance. Finally, we discuss strategies for developing future crop cultivars with enhanced NUE or PUE to advance sustainable agriculture.
ABSTRACT Nitrogen (N) and brassinosteroids (BRs) are key regulators of plant developmental plasticity in fluctuating nutrient environments, yet the direct molecular link coordinating these two signaling pathways remains elusive. Here, we report a synergistic interplay between nitrate and BR signaling that governs N utilization and lateral root development in rice (Oryza sativa L.). Nitrate activates BR response in a dose‐dependent manner, with maximal induction at 2.5 mM nitrate. Conversely, activated BR signaling enhances nitrate signaling and lateral root elongation, which strictly depends on the protein level of OsTCP19, a negative regulator of root growth. Nitrate‐induced BR signaling promotes OsTCP19 degradation within 2–4 h, while the BR signaling core kinase OsGSK2 interacts with and phosphorylates OsTCP19 at Ser141 and Thr289 to stabilize its protein. OsTCP19 directly binds to the promoters of nitrate‐responsive genes (e.g., OsNRT2.4, OsNADH‐GOGAT1, OsASN1) and root development genes (e.g., OsIAA3, OsPIN1b, OsARF19) to negatively regulate N responses and lateral root growth, respectively. Together, the OsGSK2‐OsTCP19 module establishes a direct molecular link between nitrate and BR signaling, coordinating N utilization and root plasticity in rice.
Rice blast, caused by the fungal pathogen Magnaporthe oryzae, constitutes a critical threat to global rice production. Leveraging functional genes from germplasm resources to breed resistant varieties remains the most effective and sustainable strategy for blast control. Here, we identify a GATA transcription factor, OsGATA16, as a candidate regulator of blast resistance by genome-wide association study (GWAS) using a diverse rice germplasm panel. Functional analysis shows that OsGATA16 overexpression significantly reduces blast resistance, whereas knockout lines exhibit enhanced resistance, establishing OsGATA16 as a negative regulator of rice immunity. Transcriptome, qRT-PCR, dual-luciferase, and DAP-seq assays reveal that OsGATA16 directly represses diterpenoid biosynthetic genes. UPLC-MS/MS reveals increased accumulation of pimarane-type diterpenoids in osgata16 mutants. Further analysis indicates that the key pimarane-type diterpenoid abietic acid promotes blast resistance but compromises cold tolerance. Given the known role of OsGATA16 in cold tolerance, haplotype analysis of 137 core-collection rice accessions uncovers a trade-off between blast resistance and cold tolerance. The japonica-dominant Hap1, featuring key residues Val292 and Gly333, shows stronger transcriptional repression activity than indica Hap2, with population genetics supporting divergent allele selection. Collectively, OsGATA16 negatively regulates blast resistance by repressing pimarane-type diterpenoid biosynthesis, serving as a valuable target for breeding dual stress-resilient rice.
Drought is a devastating abiotic stress that severely compromises global rice production. Despite decades of extensive research, the molecular mechanisms underlying rice drought tolerance remain largely elusive. Here, we characterize a Cys2/His2 (C2H2)-type zinc finger protein, ZFP151, as a positive transcription factor of rice drought tolerance. Mechanistically, ZFP151 directly binds to the promoter of NCED4, a rate-limiting gene in the abscisic acid (ABA) biosynthetic pathway and transcriptionally activates its expression. Through haplotype analysis of natural rice accessions, we identify five major ZFP151 haplotypes (Hap0-Hap4), among which ZFP151Hap1 is determined as the elite allele. This allele correlates with higher NCED4 expression and elevated ABA levels under drought conditions. Introgression of ZFP151Hap1, the elite allele, into the japonica cultivar Koshihikari, which carries the ZFP151Hap0 allele, significantly improves its drought tolerance. Collectively, our findings uncover the regulatory role of ZFP151 in ABA-mediated drought response and underscores its potential as a target for genetic improvement of drought-tolerant rice varieties.
Green Revolution rice varieties deliver high yields but require excessive nitrogen (N) fertilizer and show diminished N responsiveness, severely reducing nitrogen-use efficiency (NUE). To dissect the molecular basis of low N sensitivity in modern cultivars, we conducted a genome-wide association study (GWAS) for biomass response to N (BRN), a trait tightly linked to N sensitivity, using a diverse rice germplasm panel. We identified BRN1 as a key regulator of N-dependent biomass accumulation that regulates NLP3, a master transcription factor governing nitrate signaling. Under elevated N supply, the strigolactone signaling repressor D53 accumulates substantially and interacts with BRN1 to repress NLP3 transcription, thereby reducing rice N response. Notably, the high-response BRN1H allele encodes a more stable protein that alleviates D53-mediated suppression. Introgression of this allele into modern cultivars significantly enhanced N sensitivity and grain yield under both low and high N conditions. Our findings establish a D53-BRN1-NLP3 regulatory module controlling rice NUE, providing a target for rice breeding to sustain high productivity with improved resource sustainability. Here the authors show that BRN1 is a core gene modulating nitrogen-dependent growth in rice. They identify favorable BRN1 alleles that can improves rice nitrogen use efficiency and grain yield and are potentially valuable for low-nitrogen rice breeding.
Salinity stress severely limits rice productivity. Understanding how crops sustain growth during prolonged salt stress is therefore of critical importance. Here, we demonstrate that a brassinosteroid (BR)-jasmonic acid (JA) signaling network integrates nitrate signals to remodel root cell walls and promote salt recovery in rice (Oryza sativa). The GSK3-like kinase OsGSK1 interacts with and phosphorylates the transcription factor BRASSINAZOLE-RESISTANT 3 (OsBZR3), which negatively regulates root growth recovery and seedling survival under prolonged salt stress. OsBZR3 fine-tunes root cell wall thickening and compositional remodeling, as well as the nitrate response in rice under salt stress. Notably, high nitrate supply represses the salt-stress-induced phosphorylation of OsBZR3 by OsGSK1. OsBZR3 acts upstream of the JA signaling repressor Jasmonate ZIM-domain 4 (OsJAZ4) by directly binding to its promoter region. The OsGSK1-OsBZR3 module regulates OsJAZ4 activity to orchestrate the expression of downstream cell wall remodeling genes under salt stress. Our findings establish the OsGSK1-OsBZR3-OsJAZ4 module as a potential hub integrating nitrate and hormonal signals under prolonged salt stress and identify novel key genetic targets for breeding salt-resilient crops, thus advancing sustainable agricultural practices.
ABSTRACT Pre‐harvest sprouting (PHS) poses a major threat to wheat yield and quality, yet the genetic basis of seed dormancy underlying PHS resistance remains poorly understood. Here, through integrated genome‐wide association and transcriptomic analyses, we identify TaMYB7‐A1 as a key regulator of seed dormancy and PHS resistance. TaMYB7‐A1 encodes an R2R3‐MYB transcription factor that directly activates TaABI5 to modulate abscisic acid (ABA) signaling and indirectly fine‐tunes ABA–gibberellin (GA) homeostasis to enforce dormancy. Evolutionary and haplotype analyses revealed that the superior allele, TaMYB7‐A1 Hap−1 , originated from wild einkorn and was introgressed into domesticated emmer and subsequently into modern bread wheat. A miniature inverted‑repeat transposable element (MITE) insertion in its promoter substantially elevates TaMYB7‐A1 expression by increasing chromatin accessibility and facilitating the recruitment of upstream regulators, while two key amino acid substitutions (Gly23 and Gly92) strengthen its DNA‐binding and transcriptional activation capacity. Combinations of promoter and coding‐region variants generate graded PHS resistance across haplotypes, mirroring local adaptation to harvest‑season precipitation. Introgression of TaMYB7‐A1 Hap−1 into modern cultivar enhances PHS resistance without yield penalties. These findings elucidate a molecular and evolutionary framework for precipitation‐driven adaptation and provide a valuable genetic target for developing climate‐resilient wheat varieties.
Inconsistent nitrogen application rates across global croplands necessitate the adaptation of different genetic alleles to optimize nitrogen-use efficiency (NUE) in agriculture. In rice (Oryza sativa L.), different TEOSINTE BRANCHED 1, CYCLOIDEA AND PROLIFERATING CELL FACTOR 19 (OsTCP19) alleles contribute to the geographical adaptation to soil fertility. The nitrogen-sensitive allele OsTCP19-H is predominantly found in low-nitrogen regions due to its superior tillering and yield accumulation capabilities. Conversely, the nitrogen-insensitive allele OsTCP19-L is more common in nitrogen-sufficient regions, though the precise factors affecting this distribution remain unknown. Here, we report that high-nitrogen levels lead to lodging in an OsTCP19-dependent manner. Overexpression of this gene modifies plant architecture, enhancing lodging resistance in rice. Importantly, fine-tuning OsTCP19 expression can confer lodging resistance without a yield penalty. This is particularly important as it alleviates yield loss from lodging under high-nitrogen conditions and, intriguingly, can result in a substantial increase in plot yield when combined with dense planting strategies. Furthermore, the distinct nitrogen sensitivity of different OsTCP19 alleles allows for substantial improvement in grain yield and NUE under certain nitrogen conditions. Thus, our findings suggest that genetic manipulation of a single gene, OsTCP19, could allow flexible adaptation to diverse planting scenarios, maximizing genetic benefits based on local nitrogen availability.
Nitrate, a crucial nutrient and signaling molecule, is extensively studied across plants. While the NRT1.1-NLP-centered pathway dominates nitrate signaling in Arabidopsis and rice, however, whether there is functional interaction or co-regulation between the primary nitrate response (PNR) and long-term nitrogen utilization remains unclear. Here, a novel nitrate signaling pathway is identified in rice that works alongside the established ubiquitination-mediated OsNRT1.1B-OsSPX4-OsNLP3 cascade. It is demonstrated that OsCNGC14, OsCNGC16, and OsNRT1.1B form a plasma membrane-localized complex in root tips, mediating nitrate-triggered Ca2⁺ influx. The absence of either OsCNGC14 or OsCNGC16 abolished Ca2⁺ signaling and suppressed PNR. The OsNRT1.1B-OsCNGC14/16 complex activates Ca2⁺-dependent phosphorylation of OsNLP3 at Ser193, which accelerates its nuclear translocation and transcriptional activation of nitrate-responsive genes. This phosphorylation enhances both short-term PNR and long-term nitrogenutilization. This findings reveal a dual regulatory network in rice: the Ca2⁺-OsNLP3 pathway rapidly amplifies nitrate signals, while the ubiquitination-mediated OsSPX4 degradation ensures sustained nitrogen homeostasis.
Histone methylation is involved in a wide range of biological regulation in plants, and is conducted by three major components, including methyltransferases, demethylases, and histone readers. Compared with the other two components, research on histone readers is relatively limited. In this study, we demonstrate that OsSHH5 functions as an H3K9me1 reader to regulate rice disease resistance, tillering, and grain yield. Loss of OsSHH5 function significantly enhances both grain yield and disease resistance. Mechanistically, OsSHH5 recruits the H3K9 methyltransferase SGD733 and binds to H3K9me1, thereby maintaining H3K9me1 enrichment and facilitating gene silencing. In leaves, OsSHH5 interacts with the transcriptional factor HPY1 to target the resistance-related genes OsWAKg52 and OsWRKY81, maintaining their H3K9me1 levels and suppressing multiple PAMP-triggered immune responses, which ultimately reduces rice disease resistance. In tiller buds, OsSHH5 interacts with the transcriptional factor TCP19 to target the tillering-related gene OsNGR5, maintaining its H3K9me1 enrichment and inhibition of tillering, leading to reduced yield. Collectively, these findings reveal that OsSHH5 plays a vital role in integrating immune response, tillering, and grain yield in rice, providing new insights into the function of histone readers and offering a new strategy to improve rice yield and disease resistance.
Abscisic acid (ABA) is the most crucial phytohormone for plants in adapting to environmental conditions. While the ABA signaling network in plants has been extensively explored, our understanding of the diverse ABA sensing systems remains limited. Here, we found that the transcriptional response to ABA is suppressed under high-nitrate conditions but substantially increases under low-nitrate conditions, suggesting a tight integration of ABA signaling with nutrient conditions. Interestingly, NRT1.1B, traditionally recognized as a nitrate transporter and receptor, exhibits a markedly higher affinity for ABA, leading to the formation of an ABA-facilitated NRT1.1B-SPX4 complex. This complex triggers the release of SPX4-sequestered transcription factor NLP4, thereby initiating the transcriptional response to ABA. These findings establish that NRT1.1B functions as an ABA receptor. Notably, the competitive binding of nitrate and ABA to NRT1.1B unveils a mechanism that enables a flexible ABA response to fluctuating nutrient conditions, illustrating a sophisticated strategy for integrating compound environmental cues.
A recent study conducted by Hu et al. has provided novel insights into the perception of strigolactone (SL). These findings offer a comprehensive understanding of activation, termination, and regulation mechanisms involved in SL perception, all of which are crucial for the adaptation of plant architecture to fluctuations in nitrogen availability.
Nitrogen use efficiency (NUE), a critical determinant of crop productivity and agricultural sustainability, varies significantly between indica and japonica subspecies. Here, we identify three coding-region SNPs in OsNLP4 underlying this divergence. These SNPs enhance the binding affinity of OsNLP4indica to nitrate response elements (NREs), amplifying transcriptional activation of nitrogen metabolism and iron homeostasis genes. Introgression of the OsNLP4indica allele into elite japonica cultivar XS134 increases both grain yield and NUE by 12-25% across multi-location field trials under varying nitrogen regimes. Heterologous expression in Arabidopsis increases shoot biomass by 23%, demonstrating possible conservation of function in dicots. Mechanistically, the indica allele's stronger NRE-binding capacity synergistically modulates downstream pathways. Furthermore, combining OsNLP4indica with balanced nitrogen-iron fertilization boosts NUE by 30-32%. Our findings resolve a critical genetic basis of indica-japonica NUE divergence, provide a validated strategy for improving yield and NUE of commercial japonica varieties, and highlight OsNLP4indica as a cross-species genetic resource for sustainable agriculture.
Darkness is often used as an effective measure to induce leaf senescence. Although many senescence-related genes in rice have been reported, the genome-wide genetic architecture underlying leaf senescence remains poorly understood. In our study, indica and japonica rice showed contrasting responses to dark-induced leaf senescence (DILS). Genome-wide association studies (GWAS) combined with transcriptomic analyses revealed 57, 97, and 48 loci involved in the regulation of the onset, progression, and ending of DILS, respectively. Haplotype analyses showed that the senescence-related loci differentially accumulated in indica and japonica accessions and functioned additively to regulate DILS. A total of 357 candidate genes were identified that are involved in various senescence-related processes such as lipid and amino acid catabolism, photosynthesis, response to reactive oxygen species, and regulation of defence response. In addition, functional analyses of candidate genes revealed that OsMYB21 positively regulates the onset of DILS, while OsSUB1B negatively regulates its progression. Thus, our results provide new insights into the genetic regulation of DILS in rice.
Jiayang Li (李家洋)合作论文数Institute of Genetics and Developmental Biology, Chinese Academy of Sciences;Yazhouwan National Laboratory;University of Chinese Academy of Sciences10