Plants deploy sophisticated adaptive mechanisms to mitigate the detrimental effects of abiotic stresses (drought, salinity, temperature extremes, and heavy metals) and biotic stresses (pathogens and senescence) on growth and productivity. Central to these responses are transcription factors (TFs) that orchestrate stress-responsive gene networks. Among TF families, MADS-box proteins, characterized by their evolutionarily conserved DNA-binding domain, function as pivotal regulators of developmental plasticity and stress adaptation. While recent advances have clarified their roles in abiotic stress tolerance, a systematic integration of their functions in biotic stress responses has yet to be achieved. This review synthesizes current knowledge on how MADS-box TFs mediate plant adaptation to both abiotic and biotic stresses through the regulation of intricate transcriptional networks. By integrating these multifaceted insights, we advance toward a unified understanding of the molecular mechanisms by which MADS-box TFs coordinate plant responses to dual environmental challenges. Our analysis provides mechanistic insights into enhancing plant resilience through the targeted modulation of MADS-box genes and their regulatory networks. We further propose translational strategies for crop improvement, focusing on molecular breeding approaches to engineer stress-tolerant varieties that balance stress adaptation with developmental processes. This comprehensive assessment establishes MADS-box TFs as master regulators at the stress-development interface and proposes novel biotechnological avenues for sustainable agriculture.

Wheat leaf rust, caused by the biotrophic fungus Puccinia triticina (Pt), is a major threat to global wheat production. Fungal pathogens often deploy plant cell wall-degrading enzymes to breach host barriers, with glycoside hydrolases (GHs) providing hydrolytic activity and carbohydrate-binding modules (CBMs) enabling substrate recognition. However, research on their specific roles in the leaf rust fungus remains limited. Here, we functionally characterized two Pt genes, PtGH1 and PtCBM1. PtCBM1, a carbohydrate-binding module protein, binds cellulose and potentiates cellulase activity despite lacking hydrolase activity, whereas PtGH1 encodes a β-glucanase secreted via a non-classical pathway. Both proteins suppress Bax-induced cell death in Nicotiana benthamiana, suggesting immune-suppressive activity. Silencing either of the two genes in wheat via host-induced gene silencing significantly reduced fungal virulence, impaired hyphal growth, and enhanced host defense. Together, these findings identify PtGH1and PtCBM1 as distinct virulence factors that act through complementary mechanisms, involving physical facilitation and enzymatic degradation of host cell walls. This dual strategy illustrates how the leaf rust fungus overcomes host immunity and provides potential molecular targets for developing durable wheat resistance.

Broad-spectrum resistance (BSR) is highly sought after for the effective management of crop diseases. However, genes suitable for developing BSR remain scarce. In this study, we demonstrate the development of BSR to wheat yellow rust (YR), powdery mildew (PM), and leaf rust (LR) diseases elicited by three biotrophic fungal pathogens using a newly defined module, namely, RFEL1-NPR3. RFEL1 is an active RING-finger E3 ubiquitin ligase identified in diploid and polyploid wheat species, which ubiquitinates and promotes the degradation of wheat NPR3 (TaNPR3), an important negative immune regulator conserved in higher plants, via the 26S proteasome system. Downregulation of TaNPR3 by either overexpressing RFEL1 or knocking out TaNPR3 confers strong resistance against four different YR races as well as the PM and LR diseases without adverse effects on wheat growth and yield traits. Notably, the enhanced disease resistance exhibited by RFEL1-overexpressing and TaNPR3-knockout lines is correlated with increased expression of defense related genes and elevated stability of NPR1, a pivotal positive regulator of plant immune signaling. Our findings underscore the importance of ubiquitination-dependent NPR3 degradation in plant immunity and advocate for the application of the RFEL1-NPR3 module in engineering BSR against biotrophic fungal pathogens in wheat and other crops.

Wheat leaf rust, caused by Puccinia triticina (Pt), threatens global wheat production, with yield losses further exacerbated by the pathogen's evolving virulence. Although Syg1/Pho81/Xpr1 (SPX) domain-containing proteins are known regulators of phosphate homeostasis, their involvement in plant-pathogen interactions remains largely unexplored. We demonstrated that TaSPX3, a wheat SPX family gene, is rapidly induced during early Pt infection and flg22 treatment. Genetic evidence indicates that TaSPX3 is a positive regulator of rust resistance, with knockdown lines showing increased susceptibility and overexpression lines exhibiting enhanced resistance. Using yeast two-hybrid screening, we identified TaDi19-1D, a zinc finger transcription factor, as a direct TaSPX3 interactor. TaDi19-1D functions as a negative immune regulator by suppressing the expression of pathogenesis-related (PR) genes (TaPR1, TaPR2, TaPR5) through direct promoter binding. TaSPX3 counteracts this repression by physically interacting with TaDi19-1D, thereby derepressing PR gene expression and boosting wheat resistance to Pt. Our findings revealed a novel TaSPX3-TaDi19 regulatory module that fine-tunes TaPRs expression, providing mechanistic insights into pattern-triggered immunity (PTI) and potential genetic targets for breeding durable broad-spectrum disease-resistant wheat varieties.

Wheat (Triticum aestivum L.) is the most widely cultivated staple food crop globally. As a primary food source for 35–40% of the world’s population, the stability of its yield is directly linked to global food security. However, extreme weather events triggered by climate change have led to reductions in wheat yield, resulting in an urgent need to enhance the stress tolerance of wheat against drought and high temperatures. In this study, we successfully isolated and cloned a myo-inositol oxygenase gene from wheat. Further research revealed that high temperatures and drought stress significantly increased the expression level of the TaMIOXA gene in wheat leaves. A batch of overexpressing lines was obtained via Agrobacterium-mediated transformation. Compared to the control group, wheat plants with molecularly modified TaMIOXA overexpression exhibited stronger resistance to high temperatures and drought. This significantly increased their survival rates by 10% to 40%. The cumulative amount of hydrogen peroxide decreased from 7.86 × 10−4 to 1.54 × 10−2 mmol/g, and that of malondialdehyde decreased from 8.42 × 10−7 to 2.21 × 10−6 mmol/g. This confirms that overexpression of myo-inositol oxygenase significantly enhances wheat’s tolerance to drought and high temperatures. This study offers valuable genetic resources for wheat stress tolerance.

Leaf rust (Puccinia triticina) and stripe rust (Puccinia striiformis f. sp. tritici) are among the most prevalent foliar diseases in wheat, causing significant annual yield losses worldwide. To identify rust resistance genes in U.S. winter wheat, we conducted a genome-wide association study (GWAS) on resistance to leaf and stripe rusts in U.S. winter wheat cultivars and elite advanced breeding lines. Using simple sequence repeats (SSRs) and wheat 90K single nucleotide polymorphism (SNP) arrays, we identified two novel quantitative trait loci (QTLs), QLr.hwwg-2BL and QLr.hwwg-4AL, and four QTLs corresponding to known genes Lr74, Lr77, Lr18 and Lr68 for leaf rust resistance. We also identified five QTLs conferring stripe rust resistance, which included the three previously characterized loci Yr17/YrM1225 on the 2NS/2AS translocation, Yr30/Sr2 on 3BS, and QYr.hwwg-2BS, along with two putative novel loci, QYr.hwwg-2AS.2 and QYr.hwwg-4BL, with the latter located in a QTL-rich region. The QTLs identified in this study will be useful for improving durable resistance to leaf and stripe rusts in new wheat cultivars using marker-assisted gene-pyramiding strategy.

Wheat stripe rust (Puccinia striiformis f. sp. tritici, Pst) poses a catastrophic threat to global food security. While MADS-box transcription factors regulate development and abiotic stress, their roles in plant-pathogen immunity remain enigmatic. In this study, we identified TaMADS2, a Pst-induced MADS-box gene, as a positive regulator of wheat resistance. Functional analyses demonstrated that TaMADS2 overexpression significantly enhanced Pst resistance, whereas its knockdown rendered wheat more susceptible. Further investigation revealed that TaMADS2 interacts with trichome birefringence-like protein 21 (TaTBL21) to activate glycerol kinase-like (TaGKL) expression. Silencing TaGKL in wild-type or TaMADS2-overexpressing lines compromised resistance, with elevated Pst biomass. Notably, dual silencing of TaMADS2 and TaGKL further heightened susceptibility, confirming their synergistic defence role. Mechanistically, the TaMADS2-TaTBL21 complex promotes wheat resistance to stripe rust disease by upregulating TaGKL expression, leading to the accumulation of the key defence metabolites salicylic acid (SA) and glycerol-3-phosphate (G3P). Our study unveils a novel TaMADS2-TaTBL21-TaGKL module that potentiates wheat resistance against stripe rust, offering strategic targets for breeding resistant wheat.

Wheat stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), poses a significant threat to wheat production, particularly in Henan Province, which produces more than 36 million tons of wheat grain every year, the highest production among all provinces in China. This study characterized 219 Pst isolates collected from the five regions of Henan through virulence testing using two sets of wheat differentials and genotyping with 23 Kompetitive allele-specific PCR (KASP) markers developed from single nucleotide polymorphism (SNP) markers. Based on the virulence phenotypes on the Chinese differentials, 37 races were identified, including 17 new races. CYR34, CYR32, and G22-14 were the top three most prevalent races across the province. The virulence profiles varied among the five regions. The tests of the isolates with the Yr single-gene differentials revealed 75 races. None of the isolates were virulent to either Yr5 or Yr15, whereas the virulence frequencies to the other 16 Yr genes varied from 10 to 85% in the province and were slightly different among the five regions for each virulence factor. The Pst populations from the five regions were clustered into two major groups based on the two sets of differentials and the KASP-SNP marker data. These findings provide valuable insights for developing wheat cultivars with effective resistance for enhancing stripe rust management and improving wheat yields in Henan Province and the country.

Many species of the obligate biotrophic rust fungi often cause destructive diseases on crops. Glycoside hydrolases (GHs) in phytopathogens have been widely recognized for their crucial roles in breaking through the plant's defense system. Despite this, the specific functions of most GHs in rust fungi remain largely uncharted. In this study, we examined a GH26 gene from the wheat leaf rust pathogen Puccinia triticina (Pt), designated PtGH26_1, which exhibited highly induced expression during critical stages of host infection. PtGH26_1 demonstrated cellulase activity and contained a functional signal peptide, localized to both the plant cytoplasm and nucleus. When transiently expressed, PtGH26_1 inhibited Bcl2-associated X protein (Bax)-induced cell death, callose deposition, and the expression of defense-related genes in Nicotiana benthamiana. Additionally, infiltrating PtGH26_1 protein into wheat leaves compromised resistance to Pt and lessened hypersensitive responses. Silencing PtGH26_1 through host-induced gene silencing impaired fungal growth and virulence of Pt, leading to increased production of reactive oxygen species and activation of defense-related genes in wheat. Moreover, PtGH26_1 was shown to target one member of the Fantastic Four-like proteins in wheat (TaFAF), which positively regulated host resistance to Pt. Consequently, our findings indicate that PtGH26_1 is a significant virulence factor, potentially involved in breaching the barrier of plant cell walls and modulating host immune responses during Pt infection.

Wheat (Triticum aestivum L.) is the most widely cultivated staple food crop globally. As a primary food source for 35-40% of the world's population, the stability of its yield is directly linked to global food security. However, extreme weather events triggered by climate change have led to wheat yield reduction, making it an urgent issue to enhance wheat's stress tolerance against drought and high temperatures. In this study, we successfully isolated and cloned an inositol oxidase gene from wheat. Further research revealed that high-temperature and drought stresses significantly increased the expression level of the TaMIOXA gene in wheat leaves. A batch of overexpressing lines was obtained via Agrobacterium-mediated transformation. Compared with the control group, wheat plants with molecularly modified TaMIOXA overexpression exhibited stronger resistance to high temperatures and drought, with their survival rate significantly increased by 10% to 40%. This confirms that overexpression of inositol oxidase significantly enhances wheat's tolerance to drought and high temperatures.

Wheat leaf rust is caused by the obligate biotrophic fungus Puccinia triticina f. sp. tritici, which seriously affects wheat production. In this study, a novel mitovirus was identified in Puccinia triticina strain HN-1 and designated as "Puccinia triticina mitovirus 1" (PtMV1). The genome of PtMV1 consists of a single RNA molecule with a length of 2,380 nt and an A + U content of 54.7

ABSCISIC ACID-INSENSITIVE 4 (ABI4) is a pivotal transcription factor which coordinates multiple aspects of plant growth and development as well as plant responses to environmental stresses. ABI4 has been shown to be involved in regulating seedling photomorphogenesis; however, the underlying mechanism remains elusive. Here, we show that the role of ABI4 in regulating photomorphogenesis is generally regulated by sucrose, but ABI4 promotes hypocotyl elongation of Arabidopsis seedlings under blue (B) light under all tested sucrose concentrations. We further show that ABI4 physically interacts with PHYTOCHROME INTERACTING FACTOR 4 (PIF4), a well-characterized growth-promoting transcription factor, and post-translationally promotes PIF4 protein accumulation under B light. Further analyses indicate that ABI4 directly interacts with the B light photoreceptors cryptochromes (CRYs) and inhibits the interactions between CRYs and PIF4, thus relieving CRY-mediated repression of PIF4 protein accumulation. In addition, while ABI4 could directly activate its own expression, CRYs enhance, whereas PIF4 inhibits, ABI4-mediated activation of the ABI4 promoter. Together, our study demonstrates that the ABI4-PIF4 module plays an important role in mediating CRY-induced B light signaling in Arabidopsis.

DNA serves as the carrier of genetic information, with sequence variations playing a pivotal role in defining hereditary traits. Genome-Wide Association Studies (GWAS) facilitate the investigation of the links between genetic variations and phenotypes, significantly influencing biological research, particularly in animal and plant pathology. By identifying genetic markers associated with specific traits or diseases, GWAS enhances our understanding of host-pathogen interactions and improves disease-resistant breeding strategies. It has been vital in revealing the genetic basis of disease resistance, pinpointing key genes and DNA loci, which enrich genetic resources for breeding programs and deepen our knowledge of disease resistance mechanisms at the DNA level. Additionally, GWAS contributes to pathogen population genetics, facilitating a thorough exploration of pathogen virulence. Integrating GWAS with marker-assisted selection enhances breeding efficiency and precision in selecting for disease-resistant traits. While previous research has largely focused on host genetics, the genetic variation of pathogens is equally significant. Notably, reports integrating animal and plant pathosystems are still lacking. Given the importance of these systems, this review summarizes key advancements in this field, addresses current challenges, and proposes future directions, thereby offering a vital reference for ongoing research.

SPX (SYG/PHO81/XPR1) domain genes have been reported to play vital roles in the Phosphorus (Pi) signaling network in Arabidopsis thaliana and rice. However, the functions of SPX proteins in wheat remain largely unknown. In this study, the full-length cDNA sequence of the TaSPX3 gene was cloned from the common wheat variety Zhengmai9023. The expression of TaSPX3 was up-regulated in eight different genotypes of wheat under low phosphorus (LP) stress, indicating that TaSPX3 responds to Pi limitation in multiple wheat genotypes. The transcription level of TaSPX3 was also detected in the absence of seven different elements, showing certain specificity for Pi deficiency in wheat. Over expressing TaSPX3 in Arabidopsis can alleviate Pi deficiency symptoms at the seedling stage and promote the growth of plant, and advance the flowering period at the adult stage. The expression of 7 genes associated with the Pi starvation signal pathways was analyzed using qRT-PCR. The results showed that TaSPX3, along with AtSPX1, AtRNS1, AtIPS1, AtPAP2, AtPAP17 and AtAT4, were all induced by Pi deficiency. This study reveals that the TaSPX3 gene in wheat is involved in the response to phosphorus stress and may affect shoot phosphorus levels through AT4 or PAPs-related pathways. Overall, our study provides new insights into the regulation of plant response under LP conditions and the molecular mechanism underlying the role of the wheat SPX gene in coping with LP stress.

Translation elongation factors (EF) play essential roles in intracellular protein synthesis and are often used as housekeeping genes in expression studies due to their relatively steady levels, and some EF genes have also been found to participate in the stress response. At present, little information regarding stress-related EF genes is available in nutrient-induced signal transduction. Here, in order to better explore the molecular function of EF gene in response to nutrient stress, we isolated a translation elongation factor gene from the wheat cultivar ‘Zhengmai9023’, which was named TaEF1A, and its structural characteristics and sequence conservation among related species were analyzed. TaEF1A expression is rapidly induced by low phosphate (LP) stress at the early stage in wheat. Moreover, to further elucidate the function of the TaEF1 gene in the low phosphate (LP) stress response, we generated TaEF1A-overexpressing transgenic Arabidopsis thaliana plants and found that the number of lateral roots in TaEF1A-overexpressing transgenic Arabidopsis thaliana was significantly increased compared with that in wild-type plants under LP stress. Meanwhile, observations using a mCherry antibody combined with laser confocal microscopy revealed that the TaEF1A protein was distributed near the membranes of root tip cells. More importantly, analysis of the transcription level showed that the expression of the key gene auxin response factor (ARF7), which is a critical factor for lateral root primordial development, was significantly up-regulated, indicating that the TaEF1A gene might promote lateral root development by regulating the ARF gene. Taken together, our results suggest that the TaEF1A gene is involved in the response to phosphorus stress and affects lateral root development, providing new clues into the regulation of the plant response under LP and the molecular mechanism underlying the role of the wheat EF gene in the stress response.

Based on the expression of TaMADS2 gene was up-regulated by the infection of leaf rust in compatible/incompatible wheat varieties and the response period was earlier in incompatible wheat than in compatible wheat, the function of TaMADS2 in wheat resistance to leaf rust was studied by using BSMV-VIGS technology. The phenotypes of TaMADS2-silenced plants（wheat cultivars ‘Chinese Spring’ and ‘Zhengmai 9023’） and the transcriptional level changes of pathogenesis-related genes were analyzed. The results showed a significant increase in disease severity of leaf rust on BSMV-infected wheat leaves, the length of infection hypha（IH） and infection area in wheat seedlings, as well as a remarkable decrease in the accumulation of reactive oxygen species（ROS） at single infection sites in TaMADS2-silenced plants, suggesting that the growth of pathogen fungus was promoted while the disease resistance response of plant was decreased in comparison to the non-silenced plants inoculated with leaf rust. Furthermore, qRT-PCR analysis showed that the expressing levels of pathogenesis-related genes TaPR1、TaPR2 and ROS-scavenging gene TaCAT were significantly down-regulated in the early stage of rust infection. In conclusion, TaMADS2 may inhibit the infection of leaf rust and positively regulate the resistance to leaf rust by regulating the expression of pathogenesis-related genes in wheat.

Chromosome evolution drives species evolution, speciation, and adaptive radiation. Accurate genome assembly is crucial to understanding chromosome evolution of species, such as dikaryotic fungi. Rust fungi (Pucciniales) in dikaryons represent the largest group of plant pathogens, but the evolutionary process of adaptive radiation in Pucciniales remains poorly understood. Here, we report a gapless genome for the wheat leaf rust fungus Puccinia triticina determined using PacBio high-fidelity (HiFi) sequencing. This gapless assembly contains two sets of chromosomes, showing that one contig represents one chromosome. Comparisons of homologous chromosomes between the phased haplotypes revealed that highly frequent small-scale sequence divergence shapes haplotypic variation. Genome analyses of Puccinia triticina along with other rusts revealed that recent transposable element bursts and extensive segmental gene duplications synergistically highlight the evolution of chromosome structures. Comparative analysis of chromosomes indicated that frequent chromosomal rearrangements may act as a major contributor to rapid radiation of Pucciniales. This study presents the first gapless, phased assembly for a dikaryotic rust fungus and provides insights into adaptive evolution and species radiation in Pucciniales. IMPORTANCE Rust fungi (Pucciniales) are the largest group of plant pathogens. Adaptive radiation is a predominant feature in Pucciniales evolution. Chromosome evolution plays an important role in adaptive evolution. Accurate chromosome-scale assembly is required to understand the role of chromosome evolution in Pucciniales. We took advantage of HiFi sequencing to construct a gapless, phased genome for Puccinia triticina. Further analyses revealed that the evolution of chromosome structures in rust lineage is shaped by the combination of transposable element bursts and segmental gene duplications. Chromosome comparisons of Puccinia triticina and other rusts suggested that frequent chromosomal arrangements may make remarkable contributions to high species diversity of rust fungi. Our results present the first gapless genome for Pucciniales and shed light on the feature of chromosome evolution in Pucciniales.

组氨酸磷酸转运蛋白HP(histidine phosphotransfer proteins)在植物的生长发育调控及逆境胁迫应答中发挥重要作用.为理解HP基因在小麦基因组中的进化特征和功能,研究通过生物信息学分析鉴定普通小麦的HP基因家族成员,对其理化性质、进化特征、基因结构、顺式作用元件以及在逆境胁迫条件下的表达模式进行了分析.结果表明,在小麦基因组鉴定到31 个HP基因,编码蛋白质序列包括 116～200 个氨基酸.通过和其他植物的HP蛋白比较以及对蛋白结构、基因结构和基序的分析,显示小麦HP家族基因序列具有保守性.顺式作用元件预测表明,HP基因具有光、植物激素、干旱、低温等非生物胁迫响应相关的启动子调控元件.热图分析表明,HP基因在应答非生物胁迫中表达模式存在多样性;qRT-PCR分析表明,TaHP5-6B基因在低磷胁迫下受到强烈的诱导表达.综上所述,小麦全基因组鉴定的HP家族基因是非生物胁迫响应的重要基因资源.

Ovarian cancer is a gynecological tumor with an incidence rate lower than those of other gynecological tumor types and the second-highest death rate. CC chemokine 2 (CCL2) is a multifunctional factor associated with the progression of numerous cancers. However, the effect of CCL2 on ovarian cancer progression is unclear. Here, we found that exogenous CCL2 and the overexpression of CCL2 promoted the proliferation and metastasis of ovarian cancer cells. On the other hand, CCL2 knockdown via CRISPR/Cas9 inhibited ovarian cancer cell proliferation, migration, and invasion. The present study demonstrated that mitogen-activated protein three kinase 19 (MAP3K19) was the key CCL2 target for regulating ovarian cancer progression through transcriptome sequencing. Additionally, MAP3K19 knockout inhibited ovarian cancer cell proliferation, migration, and invasion. Furthermore, CCL2 increased MAP3K19 expression by activating the mitogen-activated protein kinase kinase (MEK)/extracellular signal-regulated kinase (ERK) pathway. The present study showed the correlation between CCL2 and ovarian cancer, suggesting that CCL2 may be a novel target for ovarian cancer therapy.

Viruses often usurp host machineries for their amplification, but it remains unclear if hosts may subvert virus proteins to regulate viral proliferation. Here, we show that the 17K protein, an important virulence factor conserved in barley yellow dwarf viruses (BYDVs) and related poleroviruses, is phosphorylated by host GRIK1-SnRK1 kinases, with the phosphorylated 17K (P17K) capable of enhancing the abundance of virus-derived small interfering RNAs (vsiRNAs) and thus antiviral RNAi. Furthermore, P17K interacts with barley small RNA-degrading nuclease 1 (HvSDN1) and impedes HvSDN1-catalyzed vsiRNA degradation. Additionally, P17K weakens the HvSDN1-HvAGO1 interaction, thus hindering HvSDN1 from accessing and degrading HvAGO1-carried vsiRNAs. Importantly, transgenic expression of 17K phosphomimetics (17K5D ), or genome editing of SDN1, generates stable resistance to BYDV through elevating vsiRNA abundance. These data validate a novel mechanism that enhances antiviral RNAi through host subversion of a viral virulence protein to inhibit SDN1-catalyzed vsiRNA degradation and suggest new ways for engineering BYDV-resistant crops.