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Molecular Pathogens (online), 2025, Vol. 16, No. 5 ISSN 1925-1998 http://microbescipublisher.com/index.php/mp © 2025 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Latest Content Meta-Analysis of Viral Resistance Mechanisms in Potato and Related Solanaceae Jun Wang, Qikun Huang Molecular Pathogens, 2025, Vol. 16, No. 5, 207-216 Interaction Between Wheat Roots and Microorganisms Pingping Yang, Jiong Fu Molecular Pathogens, 2025, Vol. 16, No. 5, 217-225 Improving Nitrogen Fixation in Soybean: Insights into Rhizobium Interactions Xinhua Zhou, Zhonggang Li Molecular Pathogens, 2025, Vol. 16, No. 5, 226-235 Advances in Rice Breeding for Resistance to Fungal and Bacterial Diseases Ziyi Dong, Danyan Ding Molecular Pathogens, 2025, Vol. 16, No. 5, 236-245 Root Exudates and Their Influence on Wheat Soil Microbiome Lin Liu, Xiaoqing Tang Molecular Pathogens, 2025, Vol. 16, No. 5, 246-256
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 207 Meta Analysis Open Access Meta-Analysis of Viral Resistance Mechanisms in Potato and Related Solanaceae Jun Wang, Qikun Huang Tropical Microbial Resources Research Center, Cuixi Academy of Biotechnology, Zhuji, 311800, Zhejiang, China Corresponding author: qikun.huang@cuixi.org Molecular Pathogens, 2025, Vol.16, No.5 doi: 10.5376/mp.2025.16.0021 Received: 01 Aug., 2025 Accepted: 06 Sep., 2025 Published: 14 Sep., 2025 Copyright © 2025 Wang and Huang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Wang J., and Huang Q.K., 2025, Meta-analysis of viral resistance mechanisms in potato and related solanaceae, Molecular Pathogens, 16(5): 207-216 (doi: 10.5376/mp.2025.16.0021) Abstract This study conducted a meta-analysis on the virus resistance mechanisms of potatoes and solanaceous crops, and summarized the progress and findings in related fields in recent years. This article introduces the main virus types and their hazards in potato and solanaceous crops, and analyzes the impact of virus infection on plant physiology and the difficulties faced in prevention and control. Secondly, we sort out the overall framework of plant antiviral immunity, including resistance mechanisms such as pattern-triggered immunity (PTI), effector-triggered immunity (ETI), and RNA silencing, and discuss the identification and functional mechanisms of key resistance genes (such as Rx1, etc.). On this basis, we compare the similarities and differences in virus resistance between potatoes and tomatoes, peppers, eggplants and other solanaceous crops, and explore the evolution and selection pressure of resistance genes, as well as the possibility of utilizing resistance genes across species. Furthermore, a resistance regulatory network and signaling pathway model was constructed to explain the role of multi-level regulation such as plant hormone signaling, transcription factors, and epigenetics in antiviral resistance. In addition, cases are cited to illustrate the differences in resistance performance of different varieties under multi-virus co-infection. Research shows that the rational use of resistance resources and meta-analysis methods can provide scientific basis and new strategies for the prevention and control of viral diseases in potato and solanaceous crops. Keywords Potato; Solanaceae crops; Virus resistance; Immune mechanism; Meta-analysis; Resistance genes 1 Introduction Potato is the fourth largest food crop in the world, and China is also a major potato producer and consumer. However, viral diseases have become one of the major factors restricting the production of potato and related solanaceous crops. It is reported that about 40 different viruses can infect potatoes, among which the most harmful to yield and quality include potato virus Y (PVY), virus X (PVX), and leafroll virus (PLRV). These viruses can cause plant dwarfing, leaf mosaic, leaf curling and other symptoms, leading to tuber yield reduction and degeneration, and reduced seed potato quality (Kopp et al., 2015). In recent years, research on plant antiviral immune mechanisms has made a series of progress, and people have gradually realized that plants have a complex and efficient immune system to resist virus infection. Research shows that plant resistance to viruses is often controlled by dominantly inherited disease resistance genes. Most of these genes encode nucleotide-binding-leucine-rich repeat region proteins (NLR), which can specifically recognize viral products and trigger downstream defense responses (Grech-Baran et al., 2019). Some studies have found that high temperature can weaken the function of certain disease resistance genes. For example, the resistance to viruses mediated by the tobacco N gene and pepper Tsw is significantly reduced above 30°C (Richard et al., 2020). Meta-analysis is a method of comprehensive and quantitative analysis of independent results from different studies. It is widely used in the fields of medicine and social sciences. In recent years, it has also been gradually introduced into agronomy and plant protection research. Through meta-analysis, we can integrate experimental data from different regions, varieties and experimental conditions to obtain an overall estimate of disease resistance effects and influencing factors, thereby improving the statistical power and applicability of the
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 208 conclusions. For areas such as potato and solanaceous crop virus resistance mechanisms, where research results are abundant but the results may be heterogeneous, it is of great significance to conduct meta-analysis. 2 Main virus Types and Hazards in Potato and Solanaceous Crops 2.1 Overview of common viruses Potato and solanaceous crops are susceptible to a variety of viruses, some of which are globally prevalent and cause severe losses. In potatoes, PVY is one of the viruses with the highest detection rate and the most serious harm. A survey of some potato producing areas in China showed that the PVY positive rate was as high as 94%, covering almost all samples. The detection rates of PVS and PVA have also reached approximately 50% and 44% respectively, with PVA reported to be prevalent in Guizhou, China, and PVS in Henan and Jilin provinces for the first time (Ding et al., 2021). Another important virus is PLRV (Potato Leaf Roll Virus), which can cause plant leaf curling and tuber corking and is considered one of the most devastating viruses in potatoes. In addition, pathogens such as mild mosaic virus (PVM) and spindle tuber tuber virus are also common in potatoes. In tomato crops, prominent threats include Tomato Yellow Leaf Curl Virus (TYLCV), which can cause yellowing and curling of leaves and stunted fruit development, and is widely prevalent in tropical and subtropical regions (Rashid et al., 2021); Tobacco Mosaic Virus (TMV) can infect tomatoes, peppers, etc., causing mosaic leaves and necrotic spots; Tomato Spotted Wilt Virus (TSWV) is spread through thrips, causing chlorotic rings and wilting on tomatoes and peppers. Cucumber mosaic virus (CMV), pepper mosaic virus (PepMoV), potato virus Y (PVY), etc. are common on peppers. PVY can also cause leaf mottled and deformed leaves on peppers (Xu et al., 2024). 2.2 Physiological effects of viral infection Virus infection has many adverse effects on plant growth, development and physiological metabolism. Systemic spread of viruses in plants can lead to impaired photosynthesis and nutrient transport disorders. Secondly, virus infection often induces source-sink relationship imbalance, resulting in decreased tuber or fruit yield. Studies have shown that leaf curl diseases caused by PLRV and others can significantly reduce the starch content of potato tubers. Premature plant senescence caused by viruses such as PVY and PVM also reduces tuber enlargement time and ultimately reduces yield (Manasseh et al., 2023). Virus infection can trigger plant defense responses and hormone signaling disorders. When some defense responses are too strong, they can cause damage to themselves. Typically, TMV infection of tobacco induces strong salicylic acid (SA)-dependent defense, but is accompanied by large-scale necrotic spots on leaves, inhibiting normal growth. Studies have found that the damage to the host caused by the virus is often more severe during mixed infection. For example, PVX infection alone can cause 10% to 40% yield loss, but when combined with PVA, the yield loss can be as high as 80% (Li et al., 2013). 2.3 Prevention and control difficulties and research bottlenecks The prevention and control of viral diseases in solanaceous crops has always been a difficult problem in the field of plant pathology, which is mainly reflected in the following aspects: lack of specific agents. Unlike bacterial and fungal diseases, there is currently no broad-spectrum and efficient agent for plant viruses. Virus detection and diagnosis are complex. Potato and solanaceous crops may often be infected with multiple viruses at the same time, and field symptoms are atypical, posing challenges to accurate diagnosis. Virus mutation and resistance persistence. The virus has a high mutation rate and recombination ability, and it is easy to produce new strains or recombinants and break through the original resistance of the variety. Multiple infections and synergistic effects, there are often multiple virus complex infections in the field, aggravating disease symptoms and making prevention and control more complicated. There may be synergy or competition between different viruses, posing difficulties in resistance assessment and mechanism research. 3 Overall Framework of Plant Virus Resistance Mechanisms 3.1 Non-specific immune response (PTI) mechanism PTI is the first line of defense of plant innate immunity, which is triggered by pattern recognition receptors (PRR) sensing pathogen-associated patterns (PAMPs) or damage-associated patterns (DAMPs). In antiviral immunity, although plant virus particles often parasitize within cells and do not have clear PAMPs recognized by cell surface
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 209 receptors like bacteria and fungi, studies have found that plants still have some PRRs involved in antiviral defense. Typical signaling events after PTI triggering include: reactive oxygen species (ROS) burst, calcium ion influx, initiation of MAP kinase cascade, rapid transcription of defense-related genes, etc. (Figure 1) (Necira et al., 2024). Although these responses cannot completely prevent virus replication and spread like specific resistance, they can slow down virus invasion in plants at an early stage. For example, the initial stage of PVY infection in potatoes will induce the production of peroxidase and lignin deposition in local tissues, forming physical and chemical barriers to slow down the movement of the virus (Samarskaya et al., 2022). Figure 1 Systemic response of Nicotiana benthamiana plants to inoculation with mixtures of PVX-GFP combined with dsPVY, dsGFP or control (Ctr) extract. (A) Representative plants were photographed under UV light at 7 days post-inoculation (dpi). (B) Northern blot analysis of total RNA extracted from upper leaf tissues at 7 dpi. (C) qRT-PCR was used to analyze the accumulation of PVX-GFP genomic RNA levels in the systemic leaves at 7 dpi (Adopted from Necira et al., 2024) 3.2 Specific resistance response (ETI) mechanism When a virus successfully breaks through the plant's primary defense line and enters the cell interior, the plant initiates a stronger specific resistance, known as effector-triggered immunity (ETI). ETI is usually triggered by direct or indirect recognition of pathogenic effector proteins by plant disease resistance gene products. For viruses, most resistance genes belong to the NLR immune receptor family. These NLR proteins are distributed in the cytoplasm or nucleus and contain a conserved nucleotide-binding domain and a C-terminal LRR domain, which can act as a "molecular switch": they are usually bound to ADP to maintain a dormant state. Once they recognize virus-specific effectors, they switch to ATP and undergo conformational changes, and assemble into oligomeric complexes to initiate downstream immune responses (Martin et al., 2020).
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 210 3.3 RNA silencing and small RNA regulation RNA silencing (RNAi) is one of the unique and important innate immune mechanisms in plant antivirus. Plant cells are able to recognize and eliminate exogenous viral RNA by producing small interfering RNA (siRNA), thereby achieving the effect of "RNA against RNA". After the virus invades, the double-stranded RNA (dsRNA) formed by its genome or replication intermediates will be recognized and cleaved into small fragments of 21-24 nt siRNA by the plant's Dicer-like endonuclease (Andika et al., 2015). Subsequently, these virus-derived siRNA (vsiRNA) are loaded into the RNA-induced silencing complex (RISC), directing the complex to perform sequence-specific cleavage or translational inhibition of viral RNA, thereby preventing viral proliferation. In potato materials that are resistant to PVY, high levels of accumulated PVY-specific siRNA are often detected, and their presence is closely related to reduced virus titers. RNA silencing is a universal resistance pathway against almost all RNA viruses and some DNA viruses, functioning at all stages of viral infection (Choudhary, 2021). 4 Identification and Functional Analysis of Potato Virus Resistance Genes 4.1 Mining and classification of resistance gene resources Potato's antiviral genetic resources mainly come from its wild relatives and traditional varieties. In the long process of evolution, some wild species have gradually accumulated specific resistance alleles to resist viral infections in nature. Through distant hybridization, these genes have been introduced into cultivated species, providing valuable materials for breeding. According to their mode of action, antiviral genes can be roughly divided into genes that confer high resistance (immunity), usually dominant NLR genes; genes that confer moderate resistance or disease tolerance, which may be secondary effect genes or quantitative trait loci (QTL) (Meade et al., 2020); and regulatory genes related to broad-spectrum resistance, etc. Using molecular marker-assisted selection (MAS), researchers screened and classified the resistance genes of numerous potato germplasm, and conducted PCR testing on 103 potato varieties (lines) at home and abroad. The results found that the combinations of resistance genes carried in different materials were significantly different. Some varieties contain multiple antiviral genes at the same time, showing compound resistance (Gadjiyev et al., 2020). 4.2 Progress in research on key resistance genes Among numerous antiviral genes, Rx and Ry series genes have been intensively studied due to their remarkable resistance phenotypes and wide breeding applications. The Rx1 gene is one of the earliest cloned potato antiviral NLR genes, conferring extreme resistance to PVX. As early as the 1990s, researchers isolated the Rx1 and Rx2 genes from (S. tuberosum) ssp. andigena through map-based cloning. The proteins they encode contain the typical CC-NB-LRR structure. Rx1 recognizes the PVX coat protein CP and triggers a rapid resistance response, preventing PVX from spreading in the host. Follow-up studies found that the efficiency of Rx1-mediated resistance is regulated by the intracellular RanGAP2 protein: RanGAP2 can interact with the CC domain of Rx1 (Sukarta et al., 2021) and is a cofactor necessary for Rx1 function. 4.3 Case study: research on the molecular mechanism of PVX resistance mediated by Rx1 gene In order to understand the role of resistance genes more intuitively, the Rx1-PVX interaction is used as an example for analysis. When potatoes carry the Rx1 gene, they show extreme resistance to PVX. Even if they are inoculated with high-concentration virus juice, no symptoms will appear. The virus is restricted in the plant near the contact site, and no systemic infection occurs (Figure 2) (Richard et al., 2021). At the molecular level, Rx1 is activated early in PVX invasion, and its LRR region is believed to directly or indirectly detect the coat protein (CP) of PVX. Activated Rx1 rapidly oligomerizes and recruits costimulatory factors such as RanGAP2 to form a resistance complex. Subsequently, a local HR response is generated in cells surrounding the infection site, and a very small number of infected cells undergo programmed death, "uprooting" the virus (Slootweg et al., 2010). However, unlike many HR-type disease resistances, Rx1-mediated HR is very localized and mild, and no necrotic spots can be seen on the plant macroscopically. This may be due to the fact that the downstream signal intensity of Rx1 is strictly regulated, making it sufficient to defend against viruses but not injuring innocent people.
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 211 Figure 2 Rx1 localization variants Rx1-NLS and Rx1-NES failed to block PVX-GFP infection (Adopted from Richard et al., 2021) 5 Comparison of Virus Resistance Mechanisms among Solanaceae Crops 5.1 Differences and commonalities in resistance among tomatoes, peppers, and eggplants Tomatoes and peppers are the crops with the most intensive antiviral research among the Solanaceae vegetables. The identified antiviral genes in tomatoes include: Tm-2² for TMV, Sw-5b for TSWV (both CNL proteins), Ty-1/Ty-3 for TYLCV, etc., most of which come from wild relatives. Sw-5b can recognize the viral movement protein NSₘ and trigger immunity. The resistance of peppers to TSWV mainly relies on the Tsw gene, which recognizes the viral NSs protein; it also contains Pvr4 (dominant) and pvr2 (recessive) genes, which can resist PVY. Pepper breeding often combines dominant and recessive genes to enhance resistance (Ordaz et al., 2023). There are few antiviral studies on eggplant, but some wild species show resistance to CMV. Resistance in tomatoes and peppers is often accompanied by local necrosis (HR), while potato Rx1 resistance to PVX is asymptomatic (ER). The resistance of different crops relies on NLR recognition and systemic acquired resistance (SAR) activation, showing a common signaling pathway (Chen et al., 2021). In addition, disease resistance gene clusters in different crops are often located in homologous genomic regions, indicating a common evolutionary origin. 5.2 Analysis of evolution and selection pressure of resistance genes Antiviral genes in Solanaceae crops are subject to continuous selection pressure from virus communities during the evolution process. Wild species often co-evolve with viruses in long-term arms races, resulting in high diversity and rapid evolution of resistance gene families. This is especially true for the NLR gene family, where positive selection often occurs in the LRR region, accelerating the accumulation of amino acid variations to identify constantly changing pathogenic effectors (Seong et al., 2020). For example, a comparison of allelic variations in Rx genes in multiple Solanum species found that the LRRs of Rx proteins in different species are very different, reflecting traces of directed evolution. On the other hand, some highly conserved important resistance genes may experience a bottleneck effect during the domestication process, leading to a decrease in allelic richness within cultivated species and a narrowing of the genetic basis of resistance. In Solanaceae crops,
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 212 some antiviral genes also show linked evolution. For example, pvr1 and pvr6 in peppers are located at adjacent loci and inherited together, suggesting functional differentiation that may be caused by gene duplication. Another perspective on the evolution of resistance genes is the correspondence with pathogenic mutations. For example, since the Tm-22 gene of tomato was used in TMV in the 20th century, although the virus has produced breakthrough strains, the overall resistance has been maintained for a long time. This may be attributed to the functional importance of the target recognized by Tm-22, which is difficult for the virus to circumvent through mutation without losing its pathogenicity (Rivera-Márquez et al., 2022). 5.3 Application potential of cross-species resistance genes The genetic relationship between different Solanaceae crops gives some resistance genes the potential to be transferred and exert effects across species. In fact, there has been a long history of attempts to apply antiviral genes from one crop to another. A classic example is the tobacco N gene, which was originally derived from cigarette tobacco and is resistant to TMV. It was later successfully transferred to tomatoes to create TMV-resistant tomato varieties. On the one hand, the use of transgenic means can break through the barrier of conventional hybrid incompatibility and realize the introduction of distant genes. If the potato Rx1 gene is transferred into tobacco that is highly susceptible to PVX, complete immunity to PVX can be obtained in Nicotiana benthamiana. This experiment has been verified under laboratory conditions (Richard et al., 2020). On the other hand, emerging gene editing and cross-species expression regulation technologies are also being explored. A research team from the Chinese Academy of Agricultural Sciences recently successfully activated resistance to cucumber mosaic virus (CMV) in tobacco by constructing a chimeric NLR receptor and inserting antiviral elements from Arabidopsis into the tobacco background. This result shows that immune modules of different species can be recombined and integrated to create new interdisciplinary disease resistance pathways (Du et al., 2024). 6 Resistance Regulatory Network and Signaling Pathways 6.1 Hormone signaling interactions Phytohormones play a central role in regulating disease resistance immunity, and crosstalk often occurs between different hormone pathways, which jointly determine the outcome of resistance. In the antiviral response, the salicylic acid (SA) and jasmonic acid (JA) pathways are regarded as the two dominant signals. It is generally believed that the SA pathway mediates resistance to biological infections, especially rust fungi, viruses, etc., while the JA/ethylene (ET) pathway mainly deals with chewing insects and necrotic pathogens. However, research on viral immunity has found that this binary division is not absolute. In many cases, the SA and JA pathways are involved and influence each other. For example, when TMV infects tobacco, HR triggered by the N gene is accompanied by a substantial increase in SA levels, which is necessary to establish systemically acquired resistance (SAR) (Zhu et al., 2014). Inhibiting SA synthesis makes plants more susceptible to TMV at high temperatures. In potato, reports indicate that abscisic acid (ABA) signaling may be involved in the regulation of extreme resistance responses. When comparing PVY-resistant varieties, it was found that the ABA levels and related genes of the resistant varieties changed significantly after infection. It is speculated that ABA may promote the nuclear translocation process required for resistance. In fact, one mechanism of wheat resistance to stripe rust under high temperature is the intervention of ABA signaling, indicating that ABA can play an active role in some immunity (Qian and Huang, 2025). 6.2 Transcription factors and downstream regulatory modules After resistance signals are initiated, plants coordinate defense gene expression through multiple transcription factors (TFs). Studies have shown that TFs such as WRKY, bZIP, and NAC play a central role in antiviral immunity. For example, tobacco WRKY8 and WRKY28 are induced by SA to activate PR genes, and pepper CaBP60a promotes SA synthesis to enhance disease resistance. Some TFs are also pathogenic targets. For example, the TSWV effector NSs can bind to pepper TCP21 and interfere with the JA/auxin pathway, and the Tsw gene can recognize and utilize this signal. The TF network also regulates cell wall reinforcement, programmed cell death, and accumulation of resistant metabolites. In systemic acquired resistance (SAR), NPR1 interacts with TGA factors to activate defense genes and achieve long-lasting resistance of the whole plant (Chen et al., 2019).
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 213 Small RNA also affects immune gene expression by regulating mRNA stability. In addition to using specific resistance genes, disease-resistant breeding should also pay attention to regulatory factors, such as removing negative regulatory TFs through gene editing to improve immunity, but growth and resistance need to be weighed. 6.3 Epigenetic regulation mechanism Increasing evidence shows that plant immune responses to pathogens are also regulated at the epigenetic level, including DNA methylation, histone modifications, and chromatin remodeling. These epigenetic mechanisms can dynamically regulate the expression status of disease resistance-related genes (Ramirez-Prado et al., 2021). In antiviral aspects, a significant epigenetic phenomenon is the silencing of viral DNA/genome by RNA-mediated DNA methylation (RdDM). For DNA viruses such as geminivirus (TYLCV), plants can methylate their genomes to inhibit their transcription, which has been observed during tomato resistance to TYLCV. Even for RNA viruses, siRNA produced by the RdDM pathway can cause methylation changes near host resistance genes, indirectly affecting resistance expression. A study of Arabidopsis resistance to TCV (turnip mosaic virus) found that plants with mutated DNA methyltransferase were more susceptible to the virus, suggesting that DNA methylation contributes to overall resistance. In terms of histone modifications, histone acetylation is usually associated with high gene expression, while histone deacetylation and methylation such as H3K27me3 are associated with gene silencing. In antiviral responses, histone marks in the promoter regions of some defense genes are altered (Ramirez-Prado et al., 2021). 7 Influence of Environmental and Genetic Factors on Viral Resistance 7.1 Adjustment of environmental factors The external environment, especially temperature, light, water and fertilizer conditions, etc., has a significant regulatory effect on plant antiviral immunity. The most prominent example is the temperature effect. The disease resistance of many plants is weakened under high temperatures, making it easier for viruses to infect their hosts under high temperature conditions. The Tswgene of pepper also shows low efficiency in resisting TSWV at high temperatures of 30 °C, and the plants may develop systemic symptoms rather than local restrictions. There are various mechanisms by which high temperature affects resistance: On the one hand, high temperature can inhibit ETI signals. Studies have found that the synthesis and signaling of SA in Arabidopsis are inhibited at 28 °C~30 °C, causing plants that were originally resistant to TMV to become susceptible. On the other hand, high temperature may directly affect the structural stability of NLR proteins, making them difficult to activate. Some rust-resistant NLRs in wheat are more effective at high temperatures, while the opposite is true for tobacco N genes. This is because different NLRs have different temperature sensitivities. The wheat stripe rust resistance gene Xa7 ismore resistant under high temperature conditions, suggesting that some resistance mechanisms are strengthened under high temperatures (Tatineni et al., 2016). Photoperiod and light intensity are also factors. Generally, sufficient light is beneficial for plants to accumulate resistance substances and trigger defense responses. For example, ultraviolet light can induce certain antiviral secondary metabolites (Ogneva et al., 2021; Xiong et al., 2021). Under low light conditions, there is insufficient carbohydrates in the plant, the immune response is also weakened, and the virus is more likely to expand. Water and nutrients also affect resistance indirectly by affecting plant vigor and metabolism. Drought stress is often accompanied by an increase in ABA, which may weaken the SA pathway and increase virus susceptibility. 7.2 Influence of host genetic background In addition to the environment, the plant's own genetic background, that is, the composition of other genes in the genome besides the main resistance genes, will also significantly affect the antiviral phenotype. Even if different varieties or strains carry the same primary resistance gene, their resistance expression intensity may be different, which is attributed to differences in secondary genes or regulatory elements in the background. Although all potato varieties carry the Ry gene, some varieties still show mild symptoms or low-level infection under high PVY conditions in the field. This may be because their background lacks certain cofactors that enhance resistance. Further analysis revealed that this was related to combinations of other loci in these families, and that some backgrounds may harbor potential suppressors such that resistance genes are underexpressed. Therefore, methods
Molecular Pathogens, 2025, Vol.16, No.5, 207-216 http://microbescipublisher.com/index.php/mp 214 such as backcrossing are often used in breeding to introduce resistance genes over multiple generations to eliminate adverse background effects and accumulate beneficial genes. In addition to genes, gene expression patterns in the background also play a role. The promoter methylation status and transcription level of resistance genes may be different in different genetic backgrounds, which in turn affects the strength of resistance. The developmental stage and organ identity of the host context are also critical. Many crops are more susceptible to viruses in their seedling stage and become more resistant in their mature stage, partly due to different gene expression profiles during the developmental stages. Some resistance-related genes are highly expressed in mature leaves, which enhances the resistance of adult plants. 7.3 Case analysis: study on the differences in resistance of different potato varieties under multi-virus co-infection To further illustrate the interaction of environmental and genetic factors, a case of differential resistance to multi-virus co-infection in potatoes is introduced here. In trials of late-maturing potato varieties in northern China, some studies compared the virus infection of a resistant variety A and a highly susceptible variety B under natural field conditions. The results showed that even under the natural high infection pressure of PVY, PLRV and other viruses, variety A maintained healthy growth throughout the season with no obvious symptoms and the yield was basically unaffected; while variety B showed symptoms of mosaic and curling leaves very early, and was tested to be infected with PVY, PVS and PLRV at the same time, resulting in a final tuber yield reduction of more than 50% (Figure 3). An in-depth analysis of the differences between the two varieties can be attributed to the following points: (1) different compositions of resistance genes; (2) background stress resistance; (3) differences in growth period; (4) environmental adaptability (Slater et al., 2020). Figure 3 Symptoms of Potato Virus Y infection on the cultivar Atlantic. Note the leaf mottling and the tuber necrosis (Adopted from Slater et al., 2020) Acknowledgments The authors would like to thank all teachers and colleagues who provided guidance and assistance during this research, and for the peer review's revision suggestions. Conflict of Interest Disclosure The authors confirm that the study was conducted without any commercial or financial relationships and could be interpreted as a potential conflict of interest. References Andika I., Maruyama K., Sun L., Kondō H., Tamada T., and Suzuki N., 2015, Differential contributions of plant Dicer-like proteins to antiviral defences against potato virus X in leaves and roots, The Plant Journal : for Cell and Molecular Biology, 81(5): 781-793. https://doi.org/10.1111/tpj.12770 Chen J., Mohan R., Zhang Y., Li M., Chen H., Palmer I., Chang M., Qi G., Spoel S., Mengiste T., Wang D., Liu F., and Fu Z., 2019, NPR1 promotes its own and target gene expression in plant defense by recruiting CDK81, Plant Physiology, 181: 289-304. https://doi.org/10.1104/pp.19.00124 Chen Z., Wu Q., Tong C., Chen H., Miao D., Qian X., Zhao X., Jiang L., and Tao X., 2021, Characterization of the roles of SGT1/RAR1 EDS1/NDR1 NPR1 and NRC/ADR1/NRG1 in Sw-5b-mediated resistance to tomato spotted wilt virus, Viruses, 13(8): 1447. https://doi.org/10.3390/v13081447
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Molecular Pathogens, 2025, Vol.16, No.5, 217-225 http://microbescipublisher.com/index.php/mp 217 Case Study Open Access Interaction Between Wheat Roots and Microorganisms Pingping Yang, Jiong Fu Hainan Provincial Key Laboratory of Crop Molecular Breeding, Sanya, 572025, Hainan, China Corresponding author: jiong.fu@hitar.org Molecular Pathogens, 2025, Vol.16, No.5 doi: 10.5376/mp.2025.16.0022 Received: 11 Aug., 2025 Accepted: 13 Sep., 2025 Published: 20 Sep., 2025 Copyright © 2025 Yang and Fu, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Yang P.P., and Fu J., 2025, Interaction between wheat roots and microorganisms, Molecular Pathogens, 16(5): 217-225 (doi: 10.5376/mp.2025.16.0022) Abstract The wheat rhizosphere microbial community forms a complex interaction with the root system, which has an important impact on plant nutrient absorption, growth and development, and stress resistance. Root exudates serve as chemical bridges between wheat and soil microorganisms, driving processes such as beneficial symbiosis and disease occurrence. This study systematically reviewed the structural and functional characteristics of wheat roots, the composition and ecological functions of rhizosphere microbial communities, the signal communication mechanism between roots and microorganisms, and the interaction between growth-promoting bacteria and pathogenic bacteria respectively with wheat roots. It also conducted an in-depth analysis of the interaction mechanism between wheat and Bacillus based on cases. On this basis, we discussed how soil environment and agricultural management measures regulate wheat-microbe interactions, and finally looked forward to future research directions on using wheat rhizosphere microorganisms to promote sustainable crop production. Keywords Wheat; Rhizosphere microorganisms; Root exudates; Growth-promoting bacteria; Pathogenic bacteria; Interaction mechanism 1 Introduction Wheat (Triticum aestivumL.) is one of the most important food crops in the world and plays a decisive role in ensuring human food security. However, in order to achieve high yield goals, modern agriculture has long relied on large amounts of chemical fertilizers and pesticides, resulting in increased pressure on the soil environment, reduced fertilizer utilization, and prominent disease problems. Plant roots are the bridge connecting soil and plants. As the most active area of interaction between roots and microorganisms, the wheat rhizosphere nurtures a rich microbial community. A large number of studies have shown that rhizosphere microorganisms play a key role in promoting wheat nutrient absorption, enhancing plant stress resistance, and suppressing soil-borne diseases (Zheng et al., 2021; Parunandi et al., 2023). Therefore, in-depth study of the interaction mechanism between wheat roots and microorganisms is of great significance for improving crop yields and reducing chemical inputs. In recent years, with the development of high-throughput sequencing and metagenomics, people have a deeper understanding of the structure and function of the crop rhizosphere microbiome. Previous studies have found that there are significant differences in the rhizosphere microbial communities of different wheat varieties. The domestication and breeding processes may lead to changes in the diversity and function of rhizosphere microorganisms, and the ability of some modern high-yielding varieties to enrich beneficial microorganisms has decreased (Dilla-Ermita et al., 2021; Zheng et al., 2021). At the same time, research on wheat rhizosphere interactions also faces many challenges: the rhizosphere environment is complex and changeable, microbial functional redundancy is high, and the effects of a single strain are often difficult to perform stably under field conditions. This study will systematically elaborate on the structural and functional characteristics of wheat roots, the composition and ecological functions of rhizosphere microbial communities, the signal communication mechanism between roots and microorganisms, the interaction between growth-promoting bacteria and pathogenic bacteria, and the impact of environmental and management factors. At the end, prospects for future research are proposed.
Molecular Pathogens, 2025, Vol.16, No.5, 217-225 http://microbescipublisher.com/index.php/mp 218 2 Wheat Root System Structure and Functional Characteristics 2.1 Morphological structure and development characteristics of root system The wheat root system is a typical fibrous root system, composed of primary roots and secondary roots, showing a highly branched network structure. After seed germination, radicles are first produced, and then a large number of crown roots (adventitious roots) are formed at the tiller nodes of wheat seedlings, allowing the root system to continuously expand vertically and horizontally into the soil (Figure 1) (Li et al., 2021; Wang et al., 2023). The development of wheat root system has stage characteristics: in the seedling stage, the root system is mainly formed, and in the tillering stage, the root system enters a rapid growth period, continuously increasing root length and branch number, laying the foundation for absorbing water and mineral nutrients; from heading to filling stage, root activity gradually decreases, and some old roots become lignified and functionally decline (Paz-Vidal et al., 2023). The dense root hairs of wheat roots effectively expand the rhizosphere interface and accelerate the uptake of water and nutrients. The mucus continuously secreted by the root cap and root apical meristems and the shed root edge cells also attract and regulate rhizosphere microorganisms. Figure 1 TabHLH123 is a nuclear-localized transactivator (Adopted from Wang et al., 2023) Image caption: (A) TabHLH123-GFP was transiently co-expressed with the nuclear marker H2B-mCherry in leaf cells of Nicotiana benthamiana. (B) Yeast two-hybrid assays showing transactivation activity of TabHLH123 (Adopted from Wang et al., 2023) 2.2 Chemical composition of root exudates There are a wide variety of wheat root secretions, including low-molecular substances such as sugars, organic acids, and amino acids, as well as secondary metabolites such as phenolic acids and flavonoids, and high-molecular substances such as mucilaginous substances and extracellular enzymes. Low-molecular root exudates can provide carbon sources and energy for rhizosphere microorganisms and promote the colonization of beneficial microorganisms; secondary metabolites have allelopathic and antibacterial effects and help regulate the balance of the microbial community; high-molecular slimes and enzymes improve rhizosphere soil structure and nutrient acquisition (Tsang et al., 2024). 2.3 Formation and regulation of rhizosphere microenvironment The rhizosphere is a soil micro-environment that is significantly affected by the root system and is significantly different from the surrounding soil. Wheat roots release carbon sources and signaling molecules through secretions and absorb water nutrients, forming a unique chemical gradient in the rhizosphere, such as increased carbon dioxide concentration, decreased oxygen, and pH changes (Iannucci et al., 2021). Root mucus keeps the rhizosphere moist, which is beneficial to the survival of microorganisms; microorganisms improve the nutrient status of the rhizosphere by decomposing organic matter, fixing nitrogen and decomposing phosphorus, etc. Wheat can regulate exudate composition and root hair development to shape a suitable rhizosphere microenvironment and maintain the balance of root-microbe interactions (Parunandi et al., 2023).
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