Qingbin Sun

Nuclear factor Y (NF-Y) constitutes a pivotal transcription factor family that modulates plant growth and development as well as abiotic stress responses. Oat (Avena sativa L.) is an economically vital cereal crop and a major livestock forage globally. Nevertheless, the NF-Y gene family has not yet been systematically characterized in the oat genome. Here, we identified 36 AsNF-Y genes in the oat genome and categorized them into three distinct subfamilies (NF-YA, NF-YB, and NF-YC). Phylogeny, gene structure, duplication, collinearity, and conserved motif analyses revealed high evolutionary conservation of this gene family. Additionally, the identification of diverse cis-acting regulatory elements in the promoters of AsNF-Y genes, combined with their differential expression profiles under multiple abiotic stress conditions, indicated that AsNF-Ys serve as crucial regulators in modulating oat abiotic stress tolerance. Furthermore, preliminary functional validation via the TRV-VIGS system confirmed that two candidate genes, AsNF-YC02 and AsNF-YC06, may positively regulate salt tolerance in oat. Collectively, our findings deepen the understanding of NF-Y genes in gramineous crops and supply promising candidates for the genetic improvement of oat stress tolerance and molecular breeding.

Salt stress is a major abiotic constraint limiting global crop production. Oat ( Avena sativa L.), an allohexaploid cereal renowned for robust stress tolerance, remains poorly understood in terms of the molecular mechanisms underlying its response to salt stress. Here, we perform transcriptome profiling across multiple developmental stages and tissues of oat under salt stress, and construct the co‐expression regulatory network to identify salt tolerance‐associated gene modules. Notably, 10 salt‐responsive transcription factor (SRTF) families with dynamic expression patterns are identified as core regulators, showing extensive subgenomic functional divergence, characterized by subgenome‐dominant expression, as well as subgenome‐specific duplication or loss events. Further integration with a genome‐wide association study (GWAS) of the germination rate under salt stress in 225 oat accessions identified a 3‐bp InDel variation within the duplicated gene AsWRKY49‐D2 , which specifically modulates its expression by facilitating binding of the TF AsZAT18 , with AsWRKY49‐D2 further mediating oat salt tolerance through targeted regulation of AsSOS2 and AsSOS3 . Intriguingly, the salt‐tolerant allele of AsWRKY49 is scarcely distributed in Chinese oat accessions, highlighting its considerable potential for breeding application. These results shed light on the regulatory mechanisms underlying oat salt tolerance, providing valuable information for exploring salt tolerance genes and breeding new salt‐tolerant oat varieties.

Avena fatua (weedy oat) is a globally pervasive weed, notorious for its adaptability to extreme environments and herbicide tolerance. Here, we present the 10.98-Gb hexaploid genome of A. fatua and a variation map from 768 wild and cultivated oats (A. fatua, A. sterilis and A. sativa), elucidating their genetic relationship and evolutionary history. Population genomic analyses reveal genetic connections between A. fatua and cultivated naked oats, and identify divergent regions between A. fatua and A. sativa enriched in genes associated with biotic and abiotic stresses. Among them, a herbicide-resistance locus is identified on chromosome 4D, with A. fatua accessions carrying a highly differentiated haplotype from cultivated oats. Multi-omics profiling and functional validation demonstrate that one expanded GST gene in this locus contributes significantly to oat herbicide resistance. Our study provides genomic resources for understanding A. fatua’s broad adaptability to diverse environmental conditions, facilitating the development of climate-resilient oat varieties.

Persistent activation of drought tolerance is detrimental to plant growth and development. However, the mechanism that balances plant drought tolerance and growth remains largely undetermined. Here, we constructed a comprehensive co-expression network comprising 84 transcriptome datasets associated with growth and drought tolerance in oats. Moreover, 84 functional modules and many candidate genes related to drought tolerance and growth were identified. A key candidate gene, AsHSFA2c was involved in fine-tuning the balance between drought tolerance and growth by inhibiting plant growth and positively regulating drought tolerance. Then, we determined AsDOF25 as an upstream positive regulator and AsAGO1 as the downstream target gene of AsHSFA2c. These results imply that the AsDOF25-AsHSFA2c-AsAGO1 module contributes to the balance between drought tolerance and growth in oats. Our findings and resources will facilitate the identification of key genes related to drought tolerance and further studies of the genetic basis underlying strong drought tolerance in oats.

In Arabidopsis (Arabidopsis thaliana), light and circadian clock signaling converge on PHYTOCHROME-INTERACTING FACTORS (PIFs) 4 and 5 to produce a daily rhythm of hypocotyl elongation. PIF4 and PIF5 expression is repressed at dusk by the evening complex (EC), consisting of EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX). Here, we report that ELF3 recruits the JUMONJI (JMJ) H3K4me3 demethylases JMJ17 and JMJ18 to the PIF4 and PIF5 loci in the evening to remove their H3K4me3 marks. The association of JMJ17 and JMJ18 with the 2 genomic loci depends on the EC, and the H3K4me3 marks are enriched in the elf3 and jmj17 jmj18 mutants. Half of the globally differentially expressed genes are overlapping in elf3 and jmj17 jmj18. Cleavage Under Targets and Tagmentation sequencing analysis identified 976 H3K4me3-enriched loci in elf3. Aligning the H3K4me3-enriched loci in elf3 to genes with increased expression in elf3 and jmj17 jmj18 identified 179 and 176 target loci, respectively. Half of the loci are targeted by both ELF3 and JMJ17/JMJ18. This suggests a strong connection between the 2 JMJ proteins and EC function. Our studies reveal that an array of key genes in addition to PIF4 and PIF5 are repressed by the EC through the H3K4me3 demethylation pathway.

Avena sterilis, the ancestral species of cultivated oats, is a valuable genetic resource for oat improvement. Here we generated a near-complete 10.99 Gb A. sterilis genome and a high-quality 10.89 Gb cultivated oat genome. Genome evolution analysis revealed the centromeres dynamic and structural variations landscape associated with domestication between wild and cultivated oats. Population genetic analysis of 117 wild and cultivated oat accessions worldwide detected many candidate genes associated with important agronomic traits for oat domestication and improvement. Remarkably, a large fragment duplication from chromosomes 4A to 4D harbouring many agronomically important genes was detected during oat domestication and was fixed in almost all cultivated oats from around the world. The genes in the duplication region from 4A showed significantly higher expression levels and lower methylation levels than the orthologous genes located on 4D in A. sterilis. This study provides valuable resources for evolutionary and functional genomics and genetic improvement of oat.

Light and temperature are two important environmental signals to plants. After dawn, photo-activated phytochromes translocate into the nucleus and interact with a family of negative basic helix-loop-helix PIF regulators. Subsequent phosphorylation and degradation of PIFs triggers a series of photomorphogenic responses. However, excess light can damage the photosynthetic apparatus and leads to photoinhibition. Plants acclimate to a balanced state of photomorphogenesis to avoid photodamage. Here, we show that upregulation of PIF4 expression by SHB1 and CCA1 under red light represents a desensitization step. After dawn, the highly expressed circadian clock protein CCA1 brings circadian signals to the regulatory region of the PIF4 signaling hub. Recruitment of SHB1 by CCA1 modulates red light-specific induction of PIF4 expression thus integrating circadian and light signals. As noon approaches and light intensity and ambient temperature tend to increase, the SHB1–CCA1 interaction sustains PIF4 expression to trigger thermomorphogenic responses to changing light and temperature conditions.