Comparative Transcriptome Analysis of Pine Trees Treated with Resistance-Inducing Substances against the Nematode Bursaphelenchus xylophilus

Park, Jung–Wook; Jeon, Hee Won; Jung, Hyejung; Lee, Hyun‐Hee; Kim, Junheon; Park, Ae Ran; Kim, Namgyu; Han, Gil Soo; Kim, Jin-Cheol; Seo, Young-Su

doi:10.3390/genes11091000

Cited by 12 publications

(10 citation statements)

References 93 publications

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“…Flavonoids play a key role in tree defense against the PWN through signal transduction and metabolic regulation (Isshiki et al, 2014; Vazquez-Vilar et al, 2023; Wang et al, 2024a). Following PWN invasion, the host recognizes PWN secretions and related microbial products, activates defense signaling pathways, and induces the expression of flavonoids (Park et al, 2020). These substances have antioxidant and antimicrobial functions that limit PWN pathogenicity and microbial infection (Raorane et al, 2019; Liu et al, 2023b).…”

Section: Discussionmentioning

confidence: 99%

The molecular basis of pine wilt disease resistance inPinus massoniana

Wang,

Cai,

Zeng

et al. 2024

Preprint

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Pine wilt disease (PWD), caused by the pine wood nematode (PWN)Bursaphelenchus xylophilus, results in significant economic and ecological damage toPinusforests and plantations worldwide.Pinus massonianais the primary host of PWD in southern China, but its response to the PWN remains largely unstudied. Previously, we observed PWD in aP. massoniananursery that contained over 71 commonly used cultivars. Through field phenotyping, we identified two groups of PWN resistant cultivars. Resistant cultivars (RC) exhibited very low PWN carrying amounts (PCA) and had relatively low mortality, and tolerant cultivars (TC) had high PCA but low mortality. In this study, we confirmed via PWN inoculation assays that the resistant and tolerant cultivars had lower mortality rates, 10% and 11%, respectively, than other cultivars (which had a mortality rate of 83.3%). The RC had a PCA that was significantly lower than that of other cultivars, while the TC exhibited a higher PCA. To explore the molecular mechanisms underlying the response ofP. massonianato PWN, the transcriptome and metabolome of the above cultivars were profiled by high throughput sequencing. As no reference genome is available forP. massoniana, we generated a new full-length transcriptome library with iso-seq. Using the transcriptome and metabolome from differentP. massonianacultivars inoculated with PWN, we found three major PWD resistance strategies. 1) The common response strategy involved three important molecular pathways. First, synthesis of indole-3-acetic acid (IAA) and abcisic acid (ABA) were suppressed during PWN invasion, thus suppressing the synthesis of polysaccharides (especially myo-inositol and trehalose) and (-)-riboflavin through ABC transporters. Second, by inhibiting aspartic acid, the synthesis of arginine and proline through APS5 (aspartate aminotransferase 5) were suppressed. Third, by reducing cysteine, GERD (germacrene D synthase) was up-regulated, and sesquiterpenoid and triterpenoid metabolites were accumulated to resist PWN invasion. 2) The most effective resistance strategy involved the accumulation of reactive oxygen species (ROS), which enhanced jasmonic acid (JA) accumulation and highly induced the expression of chitinase, thus improving resistance to PWN. 3) The tolerance strategy involved the induction of phosphatidylcholine, which promoted flavonoid and anthocyanin synthesis via LPIN (phosphatidate phosphatase), LOX2S (lipoxygenase), and LOX1_5 (linoleate 9S-lipoxygenase), thus significantly inhibiting the pathogenicity of the PWN but not the PCA. These results illustrate the molecular mechanisms by whichP. massonianacultivars resist or tolerate PWN and are of great significance in the prevention and control of PWD.

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Section: Discussionmentioning

confidence: 99%

The molecular basis of pine wilt disease resistance inPinus massoniana

Wang,

Cai,

Zeng

et al. 2024

Preprint

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“…Our previous studies reported genome-wide analyses of pine trees treated with MeSA against the nematode B. xylophilus ( Park et al, 2020 ). The application of the MeSA, effective in terms of reducing PWD severity, mainly induce genes involved in systems for protection from ROS damage as well as genes encoding flavonoid biosynthesis.…”

Section: Discussionmentioning

confidence: 99%

“…It has been demonstrated that MeSA can effectively control PWD by inducing flavonoid biosynthesis through comparative in vivo transcriptomics on pine seedlings ( Park et al, 2020 ). However, the establishment of optimal treatment conditions for high efficiency of MeSA and application to the field have not been reported.…”

Section: Introductionmentioning

confidence: 99%

Systemic Acquired Resistance-Mediated Control of Pine Wilt Disease by Foliar Application With Methyl Salicylate

et al. 2022

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Pine wilt disease (PWD), caused by the pinewood nematode, is the most destructive disease in pine forest ecosystems worldwide. Extensive research has been done on PWD, but effective disease management is yet to be devised. Generally, plants can resist pathogen attack via a combination of constitutive and inducible defenses. Systemic acquired resistance (SAR) is an inducible defense that occurs by the localized infection of pathogens or treatment with elicitors. To manage PWD by SAR in pine trees, we tested previously known 12 SAR elicitors. Among them, methyl salicylate (MeSA) was found to induce resistance against PWD in Pinus densiflora seedlings. In addition, the foliar applications of the dispersible concentrate-type formulation of MeSA (MeSA 20 DC) and the emulsifiable concentrate-type formulation of MeSA (MeSA 20 EC) resulted in significantly reduced PWD in pine seedlings. In the field test using 10-year-old P. densiflora trees, MeSA 20 DC showed a 60% decrease in the development of PWD. Also, MeSA 20 EC gave the best results when applied at 0.1 mM concentration 2 and 1 weeks before pinewood nematode (PWN) inoculation in pine seedlings. qRT-PCR analysis confirmed that MeSA induced the expression of defense-related genes, indicating that MeSA can inhibit and delay the migration and reproduction of PWN in pine seedlings by modulating gene expression. These results suggest that foliar application of MeSA could reduce PWD incidence by inducing resistance and provide an economically feasible alternative to trunk-injection agents for PWD management.

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“…The application of MeSA in P. densiflora and P. thunbergii seedling leaves in the form of spray one and two weeks before PWN inoculation significantly decreased disease progression when compared to seedlings without treatment [ 119 , 120 , 124 ]. Treatment of P. densiflora plants with MeSA and subsequent inoculation with PWN seem to induce genes and pathways similar to those previously associated with PWN resistance, such as PR-1 , PR-2 , PR-5 , peroxidases, extensins, flavonoid biosynthesis genes, and genes involved in ROS detoxification [ 119 , 124 ]. The expression levels of these genes were much higher in plants treated with MeSA than in non-treated plants, reinforcing their importance in achieving resistance to PWD.…”

Section: Defense Response Induced By the Application Of Phytohormones...mentioning

confidence: 99%

“…On the other hand, the trunk injection of MeJA had a small effect on improving P. densiflora resistance to PWN [ 124 ]. However, spraying P. massoniana seedlings with MeJA seems to induce the production of diterpenes and deter the insect vector Monochamus alternatus from feeding on the stems of elicited plants [ 125 ].…”

Section: Defense Response Induced By the Application Of Phytohormones...mentioning

confidence: 99%

Molecular Defense Response of Pine Trees (Pinus spp.) to the Parasitic Nematode Bursaphelenchus xylophilus

Modesto

Mendes

Carrasquinho

et al. 2022

Cells

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Pine wilt disease (PWD) is a severe environmental problem in Eastern Asia and Western Europe, devastating large forest areas and causing significant economic losses. This disease is caused by the pine wood nematode (PWN), Bursaphelenchus xylophilus, a parasitic migratory nematode that infects the stem of conifer trees. Here we review what is currently known about the molecular defense response in pine trees after infection with PWN, focusing on common responses in different species. By giving particular emphasis to resistance mechanisms reported for selected varieties and families, we identified shared genes and pathways associated with resistance, including the activation of oxidative stress response, cell wall lignification, and biosynthesis of terpenoids and phenylpropanoids. The role of post-transcriptional regulation by small RNAs in pine response to PWN infection is also discussed, as well as the possible implementation of innovative RNA-interference technologies, with a focus on trans-kingdom small RNAs. Finally, the defense response induced by elicitors applied to pine plants before PWN infection to prompt resistance is reviewed. Perspectives about the impact of these findings and future research approaches are discussed.

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Comparative Transcriptome Analysis of Pine Trees Treated with Resistance-Inducing Substances against the Nematode Bursaphelenchus xylophilus

Cited by 12 publications

References 93 publications

The molecular basis of pine wilt disease resistance inPinus massoniana

The molecular basis of pine wilt disease resistance inPinus massoniana

Systemic Acquired Resistance-Mediated Control of Pine Wilt Disease by Foliar Application With Methyl Salicylate

Molecular Defense Response of Pine Trees (Pinus spp.) to the Parasitic Nematode Bursaphelenchus xylophilus

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