Plasmodesmata Function and Callose Deposition in Plant Disease Defense.

Callose, found in the cell walls of higher plants such as ß-1,3-glucan with ß-1,6 branches, is pivotal for both plant development and responses to biotic and abiotic stressors. Plasmodesmata (PD), membranous channels linking the cytoplasm, plasma membrane, and endoplasmic reticulum of adjacent cells, facilitate molecular transport, crucial for developmental and physiological processes. The regulation of both the structural and transport functions of PD is intricate. The accumulation of callose in the PD neck is particularly significant for the regulation of PD permeability. This callose deposition, occurring at a specific site of pathogenic incursion, decelerates the invasion and proliferation of pathogens by reducing the PD pore size. Scholarly investigations over the past two decades have illuminated pathogen-induced callose deposition and the ensuing PD regulation. This gradual understanding reveals the complex regulatory interactions governing defense-related callose accumulation and protein-mediated PD regulation, underscoring its role in plant defense. This review systematically outlines callose accumulation mechanisms and enzymatic regulation in plant defense and discusses PD's varied participation against viral, fungal, and bacterial infestations. It scrutinizes callose-induced structural changes in PD, highlighting their implications for plant immunity. This review emphasizes dynamic callose calibration in PD constrictions and elucidates the implications and potential challenges of this intricate defense mechanism, integral to the plant's immune system.

Light signaling regulates root-knot nematode infection and development via HY5-SWEET signaling.

BACKGROUND: Meloidogyne incognita is one of the most important plant-parasitic nematodes and causes tremendous losses to the agricultural economy. Light is an important living factor for plants and pathogenic organisms, and sufficient light promotes root-knot nematode infection, but the underlying mechanism is still unclear. RESULTS: Expression level and genetic analyses revealed that the photoreceptor genes PHY, CRY, and PHOT have a negative impact on nematode infection. Interestingly, ELONGATED HYPOCOTYL5 (HY5), a downstream gene involved in the regulation of light signaling, is associated with photoreceptor-mediated negative regulation of root-knot nematode resistance. ChIP and yeast one-hybrid assays supported that HY5 participates in plant-to-root-knot nematode responses by directly binding to the SWEET negative regulatory factors involved in root-knot nematode resistance. CONCLUSIONS: This study elucidates the important role of light signaling pathways in plant resistance to nematodes, providing a new perspective for RKN resistance research.

Overexpression of Calcineurin B-like Interacting Protein Kinase 31 Promotes Lodging and Sheath Blight Resistance in Rice.

A breakthrough "Green Revolution" in rice enhanced lodging resistance by using gibberellin-deficient semi-dwarf varieties. However, the gibberellic acid (GA) signaling regulation on rice disease resistance remains unclear. The resistance test showed that a positive GA signaling regulator DWARF1 mutant d1 was more susceptible while a negative GA signaling regulator Slender rice 1 (SLR1) mutant was less susceptible to sheath blight (ShB), one of the major rice diseases, suggesting that GA signaling positively regulates ShB resistance. To isolate the regulator, which simultaneously regulates rice lodging and ShB resistance, SLR1 interactors were isolated. Yeast two-hybrid (Y2H), bimolecular fluorescence complementation (BiFC), and Co-IP assay results indicate that SLR1 interacts with Calcineurin B-like-interacting protein kinase 31 (CIPK31). cipk31 mutants exhibited normal plant height, but CIPK31 OXs showed semi-dwarfism. In addition, the SLR1 level was much higher in CIPK31 OXs than in the wild-type, suggesting that CIPK31 OX might accumulate SLR1 to inhibit GA signaling and thus regulate its semi-dwarfism. Recently, we demonstrated that CIPK31 interacts and inhibits Catalase C (CatC) to accumulate ROS, which promotes rice disease resistance. Interestingly, CIPK31 interacts with Vascular Plant One Zinc Finger 2 (VOZ2) in the nucleus, and expression of CIPK31 accumulated VOZ2. Inoculation of Rhizoctonia solani AG1-IA revealed that the voz2 mutant was more susceptible to ShB. Thus, these data prove that CIPK31 promotes lodging and ShB resistance by regulating GA signaling and VOZ2 in rice. This study provides a valuable reference for rice ShB-resistant breeding.

Overexpression of GmPAL Genes Enhances Soybean Resistance Against Heterodera glycines.

Soybean cyst nematode (Heterodera glycines, soybean cyst nematode [SCN]) disease adversely affects the yield of soybean and leads to billions of dollars in losses every year. To control the disease, it is necessary to study the resistance genes of the plant and their mechanisms. Isoflavonoids are secondary metabolites of the phenylalanine pathway, and they are synthesized in soybean. They are essential in plant response to biotic and abiotic stresses. In this study, we reported that phenylalanine ammonia-lyase (PAL) genes GmPALs involved in isoflavonoid biosynthesis, can positively regulate soybean resistance to SCN. Our previous study demonstrated that the expression of GmPAL genes in the resistant cultivar Huipizhi (HPZ) heidou are strongly induced by SCN. PAL is the rate-limiting enzyme that catalyzes the first step of phenylpropanoid metabolism, and it responds to biotic or abiotic stresses. Here, we demonstrate that the resistance of soybeans against SCN is suppressed by PAL inhibitor l-α-(aminooxy)-ß-phenylpropionic acid (L-AOPP) treatment. Overexpression of eight GmPAL genes caused diapause of nematodes in transgenic roots. In a petiole-feeding bioassay, we identified that two isoflavones, daidzein and genistein, could enhance resistance against SCN and suppress nematode development. This study thus reveals GmPAL-mediated resistance against SCN, information that has good application potential. The role of isoflavones in soybean resistance provides new information for the control of SCN. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Enhanced Rice Resistance to Sheath Blight through Nitrate Transporter 1.1B Mutation without Yield Loss under NH4+ Fertilization.

Nitrogen fertilization can promote rice yield but decrease resistance to sheath blight (ShB). In this study, the nitrate transporter 1.1b (nrt1.1b) mutant that exhibited less susceptibility to ShB but without compromising yield under NH4+ fertilization was screened. NRT1.1B's regulation of ShB resistance was independent of the total nitrogen concentration in rice under NH4+ conditions. In nrt1.1b mutant plants, the NH4+ application modulated auxin signaling, chlorophyll content, and phosphate signaling to promote ShB resistance. Furthermore, the findings indicated that NRT1.1B negatively regulated ShB resistance by positively modulating the expression of H+-ATPase gene OSA3 and phosphate transport gene PT8. The mutation of OSA3 and PT8 promoted ShB resistance by increasing the apoplastic pH in rice. Our study identified the ShB resistance mutant nrt1.1b, which maintained normal nitrogen use efficiency without compromising yield.

Transcriptome Analysis of GmPUB20A Overexpressing and RNA-Interferencing Transgenic Hairy Roots Reveals Underlying Negative Role in Soybean Resistance to Cyst Nematode.

Ubiquitination genes are key components of plant responses to biotic stress. GmPUB20A, a ubiquitination gene, plays a negative role in soybean resistance to soybean cyst nematode (SCN). In this study, we employed high-throughput sequencing to investigate transcriptional changes in GmPUB20A overexpressing and RNA-interfering transgenic hairy roots. Totally, 7661 differentially expressed genes (DEGs) were identified. Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses revealed that DEGs were significantly enriched in disease resistance and signal transduction pathways. In addition, silencing Glyma.15G021600 and Glyma.09G284700 by siRNA, the total number of nematodes was decreased by 33.48% and 27.47% than control plants, respectively. Further, GUS activity and reactive oxygen species (ROS) assays revealed that GmPUB20A, Glyma.15G021600, and Glyma.09G284700 respond to SCN parasitism and interfere with the accumulation of ROS in plant roots, respectively. Collectively, our study provides insights into the molecular mechanism of GmPUB20A in soybean resistance to SCN.

The Resistance of Maize to Ustilago maydis Infection Is Correlated with the Degree of Methyl Esterification of Pectin in the Cell Wall.

Common smut caused by Ustilago maydis is one of the dominant fungal diseases in plants. The resistance mechanism to U. maydis infection involving alterations in the cell wall is poorly studied. In this study, the resistant single segment substitution line (SSSL) R445 and its susceptible recurrent parent line Ye478 of maize were infected with U. maydis, and the changes in cell wall components and structure were studied at 0, 2, 4, 8, and 12 days postinfection. In R445 and Ye478, the contents of cellulose, hemicellulose, pectin, and lignin increased by varying degrees, and pectin methylesterase (PME) activity increased. The changes in hemicellulose and pectin in the cell wall after U. maydis infection were analyzed via immunolabeling using monoclonal antibodies against hemicellulsic xylans and high/low-methylated pectin. U. maydis infection altered methyl esterification of pectin, and the degree of methyl esterification was correlated with the resistance of maize to U. maydis. Furthermore, the relationship between methyl esterification of pectin and host resistance was validated using 15 maize inbred lines with different resistance levels. The results revealed that cell wall components, particularly pectin, were important factors affecting the colonization and propagation of U. maydis in maize, and methyl esterification of pectin played a role in the resistance of maize to U. maydis infection.

Starving the enemy: how plant and microbe compete for sugar on the border.

As the primary energy source for a plant host and microbe to sustain life, sugar is generally exported by Sugars Will Eventually be Exported Transporters (SWEETs) to the host extracellular spaces or the apoplast. There, the host and microbes compete for hexose, sucrose, and other important nutrients. The host and microbial monosaccharide transporters (MSTs) and sucrose transporters (SUTs) play a key role in the "evolutionary arms race". The result of this competition hinges on the proportion of sugar distribution between the host and microbes. In some plants (such as Arabidopsis, corn, and rice) and their interacting pathogens, the key transporters responsible for sugar competition have been identified. However, the regulatory mechanisms of sugar transporters, especially in the microbes require further investigation. Here, the key transporters that are responsible for the sugar competition in the host and pathogen have been identified and the regulatory mechanisms of the sugar transport have been briefly analyzed. These data are of great significance to the increase of the sugar distribution in plants for improvement in the yield.

Corrigendum: Progress in rice sheath blight resistance research.

[This corrects the article DOI: 10.3389/fpls.2023.1141697.].

Progress in rice sheath blight resistance research.

Rice sheath blight (ShB) disease poses a major threat to rice yield throughout the world. However, the defense mechanisms against ShB in rice remain largely unknown. ShB resistance is a typical quantitative trait controlled by multiple genes. With the rapid development of molecular methods, many quantitative trait loci (QTLs) related to agronomic traits, biotic and abiotic stresses, and yield have been identified by genome-wide association studies. The interactions between plants and pathogens are controlled by various plant hormone signaling pathways, and the pathways synergistically or antagonistically interact with each other, regulating plant growth and development as well as the defense response. This review summarizes the regulatory effects of hormones including auxin, ethylene, salicylic acid, jasmonic acid, brassinosteroids, gibberellin, abscisic acid, strigolactone, and cytokinin on ShB and the crosstalk between the various hormones. Furthermore, the effects of sugar and nitrogen on rice ShB resistance, as well as information on genes related to ShB resistance in rice and their effects on ShB are also discussed. In summary, this review is a comprehensive description of the QTLs, hormones, nutrition, and other defense-related genes related to ShB in rice. The prospects of targeting the resistance mechanism as a strategy for controlling ShB in rice are also discussed.

AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease.

The root-knot nematode Meloidogyne incognita is a pathogenic pest that causes severe economic loss to agricultural production by forming a parasitic relationship with its hosts. During the development of M. incognita in the host plant roots, giant cells are formed as a nutrient sink. However, the roles of sugar transporters during the giant cells gain sugar from the plant cells are needed to improve. Meanwhile, the eventual function of sugars will eventually be exported transporters (SWEETs) in nematode-plant interactions remains unclear. In this study, the expression patterns of Arabidopsis thaliana SWEETs were examined by inoculation with M. incognita at 3 days post inoculation (dpi) (penetration stage) and 18 dpi (developing stage). We found that few AtSWEETs responded sensitively to M. incognita inoculation, with the highest induction of AtSWEET1 (AT1G21460), a glucose transporter gene. Histological analyses indicated that the ß-glucuronidase (GUS) and green fluorescent protein (GFP) signals were observed specifically in the galls of AtSWEET1-GUS and AtSWEET1-GFP transgenic plant roots, suggesting that AtSWEET1 was induced specifically in the galls. Genetic studies have shown that parasitism of M. incognita was significantly affected in atsweet1 compared to wild-type and complementation plants. In addition, parasitism of M. incognita was significantly affected in atsweet10 but not in atsweet13 and atsweet14, expression of which was induced by inoculation with M. incognita. Taken together, these data prove that SWEETs play important roles in plant and nematode interactions.

Comparative transcriptome profiling reveals the importance of GmSWEET15 in soybean susceptibility to Sclerotinia sclerotiorum.

Soybean sclerotinia stem rot (SSR) is a disease caused by Sclerotinia sclerotiorum that causes incalculable losses in soybean yield each year. Considering the lack of effective resistance resources and the elusive resistance mechanisms, we are urged to develop resistance genes and explore their molecular mechanisms. Here, we found that loss of GmSWEET15 enhanced the resistance to S. sclerotiorum, and we explored the molecular mechanisms by which gmsweet15 mutant exhibit enhanced resistance to S. sclerotiorum by comparing transcriptome. At the early stage of inoculation, the wild type (WT) showed moderate defense response, whereas gmsweet15 mutant exhibited more extensive and intense transcription reprogramming. The gmsweet15 mutant enriched more biological processes, including the secretory pathway and tetrapyrrole metabolism, and it showed stronger changes in defense response, protein ubiquitination, MAPK signaling pathway-plant, plant-pathogen interaction, phenylpropanoid biosynthesis, and photosynthesis. The more intense and abundant transcriptional reprogramming of gmsweet15 mutant may explain how it effectively delayed colonization by S. sclerotiorum. In addition, we identified common and specific differentially expressed genes between WT and gmsweet15 mutant after inoculation with S. sclerotiorum, and gene sets and genes related to gmsweet15_24 h were identified through Gene Set Enrichment Analysis. Moreover, we constructed the protein-protein interaction network and gene co-expression networks and identified several groups of regulatory networks of gmsweet15 mutant in response to S. sclerotiorum, which will be helpful for the discovery of candidate functional genes. Taken together, our results elucidate molecular mechanisms of delayed colonization by S. sclerotiorum after loss of GmSWEET15 in soybean, and we propose novel resources for improving resistance to SSR.

Calcineurin B-like interacting protein kinase 31 confers resistance to sheath blight via modulation of ROS homeostasis in rice.

Sheath blight (ShB) severely threatens rice cultivation and production; however, the molecular mechanism of rice defence against ShB remains unclear. Screening of transposon Ds insertion mutants identified that Calcineurin B-like protein-interacting protein kinase 31 (CIPK31) mutants were more susceptible to ShB, while CIPK31 overexpressors (OX) were less susceptible. Sequence analysis indicated two haplotypes of CIPK31: Hap_1, with significantly higher CIPK31 expression, was less sensitive to ShB than the Hap_2 lines. Further analyses showed that the NAF domain of CIPK31 interacted with the EF-hand motif of respiratory burst oxidase homologue (RBOHA) to inhibit RBOHA-induced H2 O2 production, and RBOHA RNAi plants were more susceptible to ShB. These data suggested that the CIPK31-mediated increase in resistance is not associated with RBOHA. Interestingly, the study also found that CIPK31 interacted with catalase C (CatC); cipk31 mutants accumulated less H2 O2 while CIPK31 OX accumulated more H2 O2 compared to the wild-type control. Further analysis showed the interaction of the catalase domain of CatC with the NAF domain of CIPK31 by which CIPK31 inhibits CatC activity to accumulate more H2 O2 .

Corrigendum: Comparative genomic analysis reveals cellulase plays an important role in the pathogenicity of Setosphaeria turcica f. sp. zeae.

[This corrects the article DOI: 10.3389/fmicb.2022.925355.].

Gma-miR408 Enhances Soybean Cyst Nematode Susceptibility by Suppressing Reactive Oxygen Species Accumulation.

Soybean cyst nematode (SCN, Heterodera glycine) is a serious damaging disease in soybean worldwide, thus resulting in severe yield losses. MicroRNA408 (miR408) is an ancient and highly conserved miRNA involved in regulating plant growth, development, biotic and abiotic stress response. Here, we analyzed the evolution of miR408 in plants and verified four miR408 members in Glycine max. In the current research, highly upregulated gma-miR408 expressing was detected during nematode migration and syncytium formation response to soybean cyst nematode infection. Overexpressing and silencing miR408 vectors were transformed to soybean to confirm its potential role in plant and nematode interaction. Significant variations were observed in the MAPK signaling pathway with low OXI1, PR1, and wounding of the overexpressing lines. Overexpressing miR408 could negatively regulate soybean resistance to SCN by suppressing reactive oxygen species accumulation. Conversely, silencing miR408 positively regulates soybean resistance to SCN. Overall, gma-miR408 enhances soybean cyst nematode susceptibility by suppressing reactive oxygen species accumulation.

Functional Characterization of Ubiquitination Genes in the Interaction of Soybean-Heterodera glycines.

Ubiquitination is a kind of post-translational modification of proteins that plays an important role in plant response to biotic and abiotic stress. The response of soybean GmPUB genes to soybean cyst nematode (SCN, Heterodera glycines) infection is largely unknown. In this study, quantitative real-time PCR (qRT-PCR) was performed to detect the relative expression of 49 GmPUB genes in susceptible cultivar William 82 and resistant cultivar Huipizhi after SCN inoculation. The results show that GmPUB genes responded to cyst nematode infection at 1 day post-inoculation (dpi), 5 dpi, 10 dpi and 15 dpi. The expression levels of GmPUB16A, GmPUB20A, GmCHIPA, GmPUB33A, GmPUB23A and GmPUB24A were dramatically changed during SCN infection. Furthermore, functional analysis of these GmPUB genes by overexpression and RNAi showed that GmPUB20A, GmPUB33A and GmPUB24A negatively regulated soybean resistance under SCN stress. The results from our present study provide insights into the complicated molecular mechanism of the interaction between soybean and SCN.

Early infection response of fungal biotroph Ustilago maydis in maize.

Common smut, caused by Ustilago maydis (DC.) Corda, is a destructive fungal disease of maize worldwide; it forms large tumors, reducing corn yield and quality. However, the molecular defense mechanism to common smut in maize remains unclear. The present study aimed to use a leading maize inbred line Ye478 to analyze the response to U. maydis inoculation. The histological and cytological analyses demonstrated that U. maydis grew gradually to the host cells 6 h post-inoculation (hpi). The samples collected at 0, 3, 6, and 12 hpi were analyzed to assess the maize transcriptomic changes in response to U. maydis. The results revealed differences in hormone signaling, glycometabolism, and photosynthesis after U. maydis infection; specific changes were detected in jasmonic acid (JA), salicylic acid (SA), ethylene (ET), and abscisic acid (ABA) signaling pathways, glycolysis/gluconeogenesis, and photosystems I and II, probably related to defense response. MapMan analysis demonstrated that the differentially expressed genes between the treatment and control groups were clustered into light reaction and photorespiration pathways. In addition, U. maydis inoculation induced chloroplast swelling and damage, suggesting a significant effect on the chloroplast activity and subsequent metabolic process, especially hexose metabolism. A further genetic study using wild-type and galactinol-sucrose galactosyltransferase (gsg) and yellow-green leaf-1 (ygl-1) mutants identified that these two U. maydis-induced genes negatively regulated defense against common smut in maize. Our measurements showed the pathogen early-invasion process, and the key pathways of both chlorophyll biosynthesis and sugar transportation were critical modified in the infected maize line, thereby throwing a light on the molecular mechanisms in the maize-U. maydis interaction.

Comparative genomic analysis reveals cellulase plays an important role in the pathogenicity of Setosphaeria turcica f. sp. zeae.

Setosphaeria turcica f. sp. zeae and S. turcica f. sp. sorghi, the two formae speciales of S. turcica, cause northern leaf blight disease of corn and sorghum, respectively, and often cause serious economic losses. They have obvious physiological differentiation and show complete host specificity. Host specificity is often closely related to pathogen virulence factors, including secreted protein effectors and secondary metabolites. Genomic sequencing can provide more information for understanding the virulence mechanisms of pathogens. However, the complete genomic sequence of S. turcica f. sp. sorghi has not yet been reported, and no comparative genomic information is available for the two formae speciales. In this study, S. turcica f. sp. zeae was predicted to have fewer secreted proteins, pathogen-host interaction (PHI) genes and carbohydrate-active enzymes (CAZys) than S. turcica f. sp. sorghi. Fifteen and 20 polyketide synthase (PKS) genes were identified in S. turcica f. sp. zeae and S. turcica f. sp. sorghi, respectively, which maintained high homology. There were eight functionally annotated effector protein-encoding genes specifically in S. turcica f. sp. zeae, among which the encoding gene StCEL2 of endo-1, 4-ß-D-glucanase, an important component of cellulase, was significantly up-regulated during the interaction process. Finally, gluconolactone inhibited cellulase activity and decreased infection rate and pathogenicity, which indicates that cellulase is essential for maintaining virulence. These findings demonstrate that cellulase plays an important role in the pathogenicity of S. turcica f. sp. zeae. Our results also provide a theoretical basis for future research on the molecular mechanisms underlying the pathogenicity of the two formae speciales and for identifying any associated genes.

The Secreted Ribonuclease SRE1 Contributes to Setosphaeria turcica Virulence and Activates Plant Immunity.

During the plant infection process, pathogens can secrete several effectors. Some of the effectors are well-known for their roles in regulating plant immunity and promoting successful pathogen colonization. However, there are few studies on the ribonuclease (RNase) effectors secreted by fungi. In the present study, we discovered a secretable RNase (SRE1) in the secretome of Setosphaeria turcica that was significantly upregulated during the early stages of S. turcica infection in maize. Knockdown of SRE1 significantly reduced the virulence of S. turcica. SRE1 can induce cell death in maize and Nicotiana benthamiana. However, unlike the conventional hypersensitive response (HR) caused by other effectors, SRE1 is not dependent on its signal peptide (SP) or plant receptor kinases (such as BAK1 and SOBIR1). SRE1-induced cell death depends upon its enzymatic activity and the N-terminal ß-hairpin structure. SRE1 relies on its N-terminal ß-hairpin structure to enter cells, and then degrades plant's RNA through its catalytic activity causing cytotoxic effects. Additionally, SRE1 enhances N. benthamiana's resistance to pathogenic fungi and oomycetes. In summary, SRE1 promotes the virulence of S. turcica, inducing plant cell death and activating plant immune responses.