Defense Responses in Prickly Pear (Cucumis metuliferus) to Meloidogyne incognita: Insights from Transcriptomics and Metabolomics Analysis
Abstract
1. Introduction
2. Materials and Methods
2.1. Plant Materials and Experimental Setup
2.2. Transcriptomics Analysis of Control (CM) and Treated (CM_SNG) C. metuliferus Plants
2.2.1. RNA Extraction, Quality Control, and Sequencing from C. metuliferus Roots
2.2.2. Annotation and Functional Enrichment Analysis of Differentially Expressed Genes (DEGs)
2.2.3. Quantitative Real-Time PCR Validation
2.3. Metabolomics Analysis of Control (CM) and Treated (CM_SNG) C. metuliferus Plants Inoculated with M. incognita
2.3.1. Extraction of Metabolites
2.3.2. LC–MS Analysis
2.3.3. Principal Component Analysis (PCA), Partial Least Squares Discriminant Analysis (PLS-DA), and Orthogonal Partial Least Squares Discriminant Analysis (OPLS-DA)
2.3.4. Data Processing and Analysis
3. Results
3.1. Transcritptomics Analysis of M. incognita-Infected and Control C. metuliferus Plants
3.1.1. Overview of Gene Set Enrichment Analysis (GSEA) in M. incognita-Infected and Control C. metuliferus Plants
3.1.2. Identification of DEGs
3.1.3. GO Analysis of DEGs
3.1.4. Validation of Transcriptomics Data
3.2. Metabolomics Analysis
3.2.1. PCA Analysis
3.2.2. PLSDA Results
3.2.3. OPLSDA Results
3.2.4. Fold Change in Volcano Plot Analysis
3.2.5. Metabolite Expression Status in C. metuliferus Plants in Response to M. incognita
3.2.6. Identification of Key Metabolites with High Importance and Rank Frequency
3.2.7. KEGG Pathway Enrichment of Metabolites
3.3. Combined Analysis of Transcriptomics and Metabolomics
3.3.1. GO Analysis
3.3.2. KOG (Eukaryotic Orthologous Groups) Analysis
3.3.3. KEGG Pathway Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Jeger, M.; Bragard, C.; Caffier, D.; Candresse, T.; Chatzivassiliou, E.; Dehnen-Schmutz, K.; Gilioli, G.; Grégoire, J.-C.; Miret, J.A.J.; MacLeod, A.; et al. Pest categorisation of Nacobbus aberrans. EFSA J. 2018, 16, e05249. [Google Scholar] [CrossRef]
- Hemmati, S.; Saeedizadeh, A. Root-knot nematode, Meloidogyne javanica, in response to soil fertilization. Braz. J. Biol. 2020, 80, 621–630. [Google Scholar] [CrossRef]
- Cao, Y.; Lu, N.; Yang, D.; Mo, M.; Zhang, K.Q.; Li, C.; Shang, S. Root-knot nematode infections and soil characteristics significantly affected microbial community composition and assembly of tobacco soil microbiota: A large-scale comparison in tobacco-growing areas. Front. Microbiol. 2023, 14, 1282609. [Google Scholar] [CrossRef]
- Huang, K.; Jiang, Q.; Liu, L.; Zhang, S.; Liu, C.; Chen, H.; Ding, W.; Zhang, Y. Exploring the key microbial changes in the rhizosphere that affect the occurrence of tobacco root-knot nematodes. AMB Express 2020, 10, 72. [Google Scholar] [CrossRef]
- Xu, C.; Han, X.; Staehelin, C.; Zhang, J. First report of Meloidogyne arenaria on roots of Grona triflora in Guangdong Province, China. Plant Dis. 2021, 105, 3763. [Google Scholar] [CrossRef]
- Khan, M.R.; Ahamad, F. Incidence of root-knot nematode (Meloidogyne graminicola) and resulting crop losses in paddy rice in northern India. Plant Dis. 2020, 104, 186–193. [Google Scholar] [CrossRef]
- Leonetti, P.; Molinari, S. Epigenetic and metabolic changes in root-knot nematode-plant interactions. Int. J. Mol. Sci. 2020, 21, 7759. [Google Scholar] [CrossRef]
- Šeregelj, V.; Šovljanski, O.; Tumbas Šaponjac, V.; Vulić, J.; Ćetković, G.; Markov, S.; Čanadanović-Brunet, J. Horned melon (Cucumis metuliferus E. Meyer Ex. Naudin)—Current knowledge on its phytochemicals, biological benefits, and potential applications. Processes 2022, 10, 94. [Google Scholar] [CrossRef]
- Ferrara, L. A fruit to discover: Cucumis metuliferus E. Mey Ex Naudin (Kiwano). Clin. Nutr. Metab. 2018, 5, 1–2. [Google Scholar] [CrossRef]
- Usman, J.G.; Sodipo, O.A.; Kwaghe, A.V.; Sandabe, U.K. Uses of Cucumis metuliferus: A review. Cancer Biol. 2015, 5, 24–34. [Google Scholar]
- Vieira, P.; Gleason, C. Plant-parasitic nematode effectors—Insights into their diversity and new tools for their identification. Curr. Opin. Plant Biol. 2019, 50, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Thakur, S.; Rana, A.; Sharma, A.; Yangchan, J.; Choudhary, K.; Kumar, R.; Sharma, D. Plant nematode interaction and omics: A focus on Meloidogyne incognita. J. Crop Health 2024, 76, 1281–1291. [Google Scholar] [CrossRef]
- Habteweld, A.; Kantor, M.; Kantor, C.; Handoo, Z. Understanding the dynamic interactions of root-knot nematodes and their host: Role of plant growth promoting bacteria and abiotic factors. Front. Plant Sci. 2024, 15, 1377453. [Google Scholar] [CrossRef] [PubMed]
- Dhankher, O.P.; Foyer, C.H. Climate resilient crops for improving global food security and safety. Plant Cell Environ. 2018, 41, 877–884. [Google Scholar] [CrossRef]
- Holbein, J.; Grundler, F.M.W.; Siddique, S. Plant basal resistance to nematodes: An update. J. Exp. Bot. 2016, 67, 2049–2061. [Google Scholar] [CrossRef]
- Postnikova, O.A.; Hult, M.; Shao, J.; Skantar, A.; Nemchinov, L.G. Transcriptome analysis of resistant and susceptible alfalfa cultivars infected with root-knot nematode Meloidogyne incognita. PLoS ONE 2015, 10, e0118269. [Google Scholar] [CrossRef]
- Xing, X.; Li, X.; Zhang, M.; Wang, Y.; Liu, B.; Xi, Q.; Zhao, K.; Wu, Y.; Yang, T. Transcriptome analysis of resistant and susceptible tobacco (Nicotiana tabacum) in response to root-knot nematode Meloidogyne incognita infection. Biochem. Biophys. Res. Commun. 2017, 482, 1114–1121. [Google Scholar] [CrossRef]
- Shukla, N.; Yadav, R.; Kaur, P.; Rasmussen, S.; Goel, S.; Agarwal, M.; Jagannath, A.; Gupta, R.; Kumar, A. Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-infected tomato (Solanum lycopersicum) roots reveals complex gene expression profiles and metabolic networks of both host and nematode during susceptible and resistance responses. Mol. Plant Pathol. 2018, 19, 615–633. [Google Scholar] [CrossRef]
- Macharia, T.N.; Bellieny-Rabelo, D.; Moleleki, L.N. Transcriptome profiling of potato (Solanum tuberosum) responses to root-knot nematode (Meloidogyne javanica) infestation during a compatible interaction. Microorganisms 2020, 8, 1443. [Google Scholar] [CrossRef]
- Petitot, A.S.; Dereeper, A.; Silva, C.D.; Guy, J.; Fernandez, D. Analyses of the root-knot nematode (Meloidogyne graminicola) transcriptome during host infection highlight specific gene expression profiling in resistant rice plants. Pathogens 2020, 9, 644. [Google Scholar] [CrossRef]
- Zhou, Y.; Zhao, D.; Shuang, L.; Xiao, D.; Xuan, Y.; Duan, Y.; Chen, L.; Wang, Y.; Liu, X.; Fan, H.; et al. Transcriptome analysis of rice roots in response to root-knot nematode infection. Int. J. Mol. Sci. 2020, 21, 848. [Google Scholar] [CrossRef]
- Zhang, M.; Zhang, H.; Tan, J.; Huang, S.; Chen, X.; Jiang, D.; Xiao, X. Transcriptome analysis of eggplant root in response to root-knot nematode infection. Pathogens 2021, 10, 470. [Google Scholar] [CrossRef]
- Wang, Z.; Wang, W.; Wu, W.; Wang, H.; Zhang, S.; Ye, C.; Guo, L.; Wei, Z.; Huang, H.; Liu, Y.; et al. Integrated analysis of transcriptome, metabolome, and histochemistry reveals the response mechanisms of different ages P. notoginseng to root-knot nematode infection. Front. Plant Sci. 2023, 14, 1258316. [Google Scholar] [CrossRef] [PubMed]
- Sung, Y.W.; Kim, J.; Yang, J.W.; Shim, D.; Kim, Y.H. Transcriptome-based comparative expression profiling of sweet potato during a compatible response with root-knot nematode Meloidogyne incognita infection. Genes 2023, 14, 2074. [Google Scholar] [CrossRef]
- Kantor, M.; Levi, A.; Thies, J.; Guner, N.; Kantor, C.; Parnham, S.; Boroujerdi, A. NMR analysis reveals a wealth of metabolites in root-knot nematode resistant roots of watermelon plants. J. Nematol. 2018, 50, 303–316. [Google Scholar] [CrossRef] [PubMed]
- Howe, G.T.; Horvath, D.P.; Dharmawardhana, P.; Priest, H.D.; Mockler, T.C.; Strauss, S.H. Extensive transcriptome changes during the natural onset and release of vegetative bud dormancy in Populus. Front. Plant Sci. 2015, 6, 989. [Google Scholar] [CrossRef]
- Seo, Y.; Kim, Y.H. Pathological interrelations of soil-borne diseases in cucurbits caused by Fusarium species and Meloidogyne incognita. Plant Pathol. J. 2017, 33, 410–423. [Google Scholar] [CrossRef]
- Miao, G.P.; Han, J.; Zhang, K.G.; Wang, S.C.; Wang, C.R. Protection of melon against Fusarium wilt-root knot nematode complex by endophytic fungi Penicillium brefeldianum HS-1. Symbiosis 2019, 77, 83–89. [Google Scholar] [CrossRef]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef]
- Conesa, A.; Götz, S.; García-Gómez, J.; Terol, J.; Talon, M.; Robles, M. BLAST2GO: A universal tool for annotation, visualization, and analysis in functional genomics research. Bioinformatics 2005, 21, 3674–3676. [Google Scholar] [CrossRef]
- Kanehisa, M.; Araki, M.; Goto, S.; Hattori, M.; Hirakawa, M.; Itoh, M.; Katayama, T.; Kawashima, S.; Okuda, S.; Tokimatsu, T.; et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008, 36, 480–484. [Google Scholar] [CrossRef]
- Zhang, S.; Nie, L.; Zhao, W.; Cui, Q.; Wang, J.; Duan, Y.; Ge, C. Metabolomic analysis of the occurrence of bitter fruits on grafted oriental melon plants. PLoS ONE 2019, 14, e0223707. [Google Scholar] [CrossRef] [PubMed]
- Kumari, C.; Dutta, T.K.; Banakar, P.; Rao, U. Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice. Sci. Rep. 2016, 6, 22846. [Google Scholar] [CrossRef] [PubMed]
- Sato, K.; Uehara, T.; Holbein, J.; Sasaki-Sekimoto, Y.; Gan, P.; Bino, T.; Shirasu, K. Transcriptomic Analysis of Resistant and Susceptible Responses in a New Model Root-Knot Nematode Infection System Using Solanum torvum and Meloidogyne arenaria. Front. Plant Sci. 2021, 12, 680151. [Google Scholar] [CrossRef]
- Ali, M.A.; Abbas, A.; Sajjad, M.; Khan, M.A. WRKY transcription factors and plant defense responses: Current perspectives. Int. J. Agri. Biol. 2015, 17, 617–626. [Google Scholar] [CrossRef]
- Balestrini, R.; Rosso, L.C.; Veronico, P.; Melillo, M.T.; De Luca, F.; Fanelli, E.; Pentimone, I. Transcriptomic responses to water deficit and nematode infection in mycorrhizal tomato roots. Front. Microbiol. 2019, 10, 1807. [Google Scholar] [CrossRef]
- Kyndt, T.; Denil, S.; Haegeman, A.; Trooskens, G.; De Meyer, T.; Van Criekinge, W.; Gheysen, G. Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol. 2012, 196, 887–900. [Google Scholar] [CrossRef]
- Ling, J.; Mao, Z.; Zhai, M.; Zeng, F.; Yang, Y.; Xie, B. Transcriptome Profiling of Cucumis metuliferus Infected by Meloidogyne incognita Provides New Insights into Putative Defense Regulatory Network in Cucurbitaceae. Sci. Rep. 2017, 7, 3544. [Google Scholar] [CrossRef]
- Erb, M.; Kliebenstein, D.J. Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy. Plant Physiol. 2020, 184, 39–52. [Google Scholar] [CrossRef]
- Ayyanath, M.M.; Shukla, M.R.; Sriskantharajah, K.; Hezema, Y.S.; Saxena, P.K. Stable indoleamines attenuate stress—A novel paradigm in tryptophan metabolism in plants. J. Pineal Res. 2024, 76, e12938. [Google Scholar] [CrossRef]
- Arraes, F.B.; Vasquez, D.D.; Tahir, M.; Pinheiro, D.H.; Faheem, M.; Freitas-Alves, N.S.; Grossi-de-Sa, M.F. Integrated omic approaches reveal molecular mechanisms of tolerance during soybean and Meloidogyne incognita interactions. Plants 2022, 11, 2744. [Google Scholar] [CrossRef]
- Nadarajah, K.K. ROS homeostasis in abiotic stress tolerance in plants. Int. J. Mol. Sci. 2020, 21, 5208. [Google Scholar] [CrossRef]
- Zhao, J.; Sun, Q.; Quentin, M.; Ling, J.; Abad, P.; Zhang, X.; Xie, B. A Meloidogyne incognita C-type lectin effector targets plant catalases to promote parasitism. New Phytol. 2021, 232, 2124–2137. [Google Scholar] [CrossRef]
- Zhang, X.; Song, M.; Gao, L.; Tian, Y. Metabolic variations in root tissues and rhizosphere soils of weak host plants potently lead to distinct host status and chemotaxis regulation of Meloidogyne incognita in intercropping. Mol. Plant Pathol. 2024, 25, e13396. [Google Scholar] [CrossRef]
Gene ID | log2 Fold Change | p-Value | Symbol | Description |
---|---|---|---|---|
PI0020800.1 | 2.191098588 | 1.68 × 10−11 | At2g19810 | PREDICTED: zinc finger CCCH-domain-containing protein 20-like [Cucumis melo] |
PI0027185.1 | −2.149417259 | 2.50 × 10−11 | BHLH25 | PREDICTED: transcription factor bHLH18-like [Cucumis melo] |
PI0013166.1 | 1.388574244 | 6.07 × 10−11 | CYCU2-1 | PREDICTED: cyclin-U2-1 [Cucumis melo] |
PI0023141.1 | −2.071705157 | 5.06 × 10−9 | BHLH19 | PREDICTED: transcription factor bHLH18-like [Cucumis melo] |
PI0009242.1 | 3.242508934 | 1.75 × 10−8 | PATROL1 | PREDICTED: uncharacterized protein LOC103490971 [Cucumis melo] |
PI0021520.1 | 1.996070545 | 8.48 × 10−7 | PER18 | PREDICTED: peroxidase 18 [Cucumis melo] |
PI0002150.1 | −2.590812197 | 1.66 × 10−6 | At3g43660 | PREDICTED: vacuolar iron transporter homolog 2-like [Cucumis melo] |
PI0002806.1 | −4.3941469 | 1.68 × 10−6 | DTX42 | PREDICTED: protein DETOXIFICATION 43-like [Cucumis melo] |
PI0018265.1 | −1.885021592 | 2.17 × 10−6 | QWRF2 | PREDICTED: QWRF motif-containing protein 2 [Cucumis melo] |
PI0025339.1 | 2.622356119 | 3.10 × 10−6 | OMT3 | Trans-resveratrol di-O-methyltransferase-like [Cucumis melo var. makuwa] [Cucumis melo] |
PI0014793.1 | 3.031698979 | 3.18 × 10−6 | P4H3 | PREDICTED: probable prolyl 4-hydroxylase 3 isoform X2 [Cucumis melo] |
PI0013781.1 | 1.763819924 | 4.87 × 10−6 | At3g27220 | PREDICTED: kelch repeat-containing protein At3g27220-like [Cucumis melo] |
PI0017889.1 | 2.725058148 | 4.93 × 10−6 | AAO | PREDICTED: L-ascorbate oxidase-like [Cucumis melo] |
PI0006726.1 | 2.066443737 | 5.27 × 10−6 | TPPJ | PREDICTED: probable trehalose-phosphate phosphatase J [Cucumis melo] |
PI0025578.1 | 1.796661262 | 6.51 × 10−6 | S-ACP-DES6 | Stearoyl-(acyl-carrier-protein) 9-desaturase 6 [Cucumis melo var. makuwa] [Cucumis melo] |
PI0006807.1 | −1.123664144 | 7.96 × 10−6 | BRH1 | Zinc finger protein [Cucumis melo var. makuwa] [Cucumis melo] |
PI0022271.2 | 1.464858379 | 1.11 × 10−5 | TIR1 | PREDICTED: protein TRANSPORT INHIBITOR RESPONSE 1 [Cucumis melo] |
PI0019118.3 | 2.319823364 | 1.30 × 10−5 | At1g08570 | PREDICTED: thioredoxin-like 1-2, chloroplastic [Cucumis melo] |
PI0016220.1 | 1.56481684 | 1.94 × 10−5 | ANS | PREDICTED: 1-aminocyclopropane-1-carboxylate oxidase 5 isoform X1 [Cucumis melo] |
PI0024504.1 | −0.86209535 | 2.45 × 10−5 | At5g22810 | PREDICTED: GDSL esterase/lipase At5g22810 [Cucumis melo] |
PI0007042.1 | 3.217055617 | 3.11 × 10−5 | ZHD11 | PREDICTED: zinc-finger homeodomain protein 9 [Cucumis melo] |
PI0027455.1 | 2.127480529 | 3.41 × 10−5 | AUX22D | PREDICTED: auxin-induced protein 22D-like [Cucumis melo] |
PI0001538.1 | −1.10242728 | 3.95 × 10−5 | SERINC3 | PREDICTED: serine incorporator 3 [Cucumis melo] |
PI0016478.1 | 1.23938667 | 4.27 × 10−5 | At5g24760 | PREDICTED: alcohol dehydrogenase-like 6 [Cucumis melo] |
PI0027502.1 | 2.735641413 | 4.50 × 10−5 | At2g24130 | PREDICTED: putative leucine-rich repeat receptor-like serine/threonine-protein kinase At2g24130 [Cucumis melo] |
PI0024420.1 | 1.539240236 | 5.38 × 10−5 | qtrt1 | PREDICTED: queuine tRNA-ribosyltransferase-like isoform X1 [Cucumis melo] |
PI0007226.1 | 1.348112951 | 7.13 × 10−5 | EXPA1 | PREDICTED: expansin-A1 [Cucumis melo] |
PI0004383.1 | 1.326878899 | 7.27 × 10−5 | IQM3 | PREDICTED: IQ domain-containing protein IQM3 [Cucumis melo] |
PI0006849.1 | 3.064955442 | 8.55 × 10−5 | ADS3 | PREDICTED: palmitoyl-monogalactosyldiacylglycerol delta-7 desaturase, chloroplastic-like [Cucumis melo] |
PI0013752.1 | 1.553329923 | 0.000104 | TCP20 | PREDICTED: transcription factor TCP20-like [Cucumis melo] |
PI0023307.1 | 2.26174537 | 0.000109 | ADH1 | alcohol dehydrogenase 1 [Cucumis melo var. makuwa] [Cucumis melo] |
PI0021014.1 | 2.149025208 | 0.000111 | Reg-2 | Haloacid dehalogenase-like hydrolase domain-containing protein 3 [Cucumis melo var. makuwa] [Cucumis melo] |
PI0025553.1 | 1.910088879 | 0.000115 | SAUR72 | PREDICTED: auxin-responsive protein SAUR64 [Cucumis melo] |
PI0000301.1 | 2.056523164 | 0.000118 | ATJ8 | PREDICTED: chaperone protein dnaJ 8, chloroplastic [Cucumis melo] |
PI0021996.1 | 1.511961146 | 0.000123 | PERK1 | PREDICTED: probable LRR receptor-like serine/threonine-protein kinase At5g10290 [Cucumis melo] |
PI0001566.1 | −3.438510233 | 0.000135 | EIX1 | PREDICTED: probable LRR receptor-like serine/threonine-protein kinase At4g36180 [Cucumis melo] |
PI0016064.1 | 1.785878749 | 0.000149 | PUB27 | PREDICTED: U-box domain-containing protein 27 [Cucumis melo] |
PI0008364.1 | 1.895530733 | 0.000177 | VUP1 | PREDICTED: uncharacterized protein LOC103495948 [Cucumis melo] |
PI0019164.1 | −2.625432617 | 0.000198 | IPT5 | PREDICTED: adenylate isopentenyltransferase 5, chloroplastic-like [Cucumis melo] |
Primer ID | Primer Sequence (5′ to 3′) |
---|---|
ERF008-F | TTCCTTGTTGTTCTTCTTGTT |
ERF008-R | AGTCGCCATCTGAATCTT |
MYB73-F | CGAAGTGAGGAAGTACAT |
MYB73-R | CCATACGCTTAACAACAG |
PAT-F | CTTCCAACGCATATAGACAA |
PAT-R | TTCATCAGACAGCACAGA |
PHI-1-F | TTCTTCTTCTTCTTCTTCTT |
PHI-1-R | TATGTGACGATTGGTTAG |
PUB19-F | AATCCTTCTCGCATTCTT |
PUB19-R | TCCTCCAACAGATACAGA |
RLP51-F | GGAGTGATGAGAATGATG |
RLP51-R | CTTGGATAAGAGAACAGAA |
TLP-F | CCAGTGATTATACGAAGTT |
TLP-R | CCAGTAGAAGGACACATA |
WRKY33-F | ATGATTATGAGGAGGTTGAC |
WRKY33-R | TGGAAGAAGAGGACTGAA |
Cm (ID: c168675_g9)-F | ATCCACGAAACTACTTACAACTCC |
Cm (ID: c168675_g9)-R | ATAGACCCTCCAATCCAGACAC |
Metabolites | Control Mean | Infected Mean | Dominance | log2(FC) | p-Value |
---|---|---|---|---|---|
All trans retinal | 0.101535431 | 0.311489633 | treatment | 1.6172 | 0.007029 |
Lappaconitine | 0.018293772 | 0.092140971 | treatment | 2.3325 | 0.007117 |
Ganoderic acid C6 | 0.158904236 | 0.047436385 | control | −1.7441 | 0.007313 |
3-phenyl-5-[3-(trifluoromethyl)-1H-pyrazol-1-yl]-1,2,4-thiadiazole | 1.145579956 | 0.257296513 | control | −2.1546 | 0.007686 |
Alprazolam-d5 | 0.259255785 | 1.427059707 | treatment | 2.4606 | 0.00811 |
Carbaprostacyclin | 0.975345612 | 0.096032635 | control | −3.3443 | 0.008338 |
1-(2,4-difluorobenzoyl)-4-piperidinecarboxylic acid | 1.667132687 | 5.529450855 | treatment | 1.7298 | 0.008526 |
Pomolic acid beta-D-glucopyranosyl ester | 0.289677297 | 1.022428149 | treatment | 1.8195 | 0.009681 |
Thymine | 2.838536724 | 7.464759358 | treatment | 1.3949 | 0.012748 |
2′-Deoxyinosine | 0.211892736 | 1.565708163 | treatment | 2.8854 | 0.0137 |
Stachydrine | 1.854910366 | 4.959460711 | treatment | 1.4188 | 0.01381 |
Aleuritic acid | 0.112353357 | 0.302231114 | treatment | 1.4276 | 0.014773 |
Biocytin | 0.233994102 | 0.706542651 | treatment | 1.5943 | 0.016332 |
Trillin | 0.090255146 | 0.489521353 | treatment | 2.4393 | 0.0184 |
Cortisol | 1.701506052 | 4.799858874 | treatment | 1.4962 | 0.019333 |
MAG (18:3) | 3.221848182 | 8.325305253 | treatment | 1.3696 | 0.019676 |
16-Heptadecyne-1,2,4-triol | 0.474532408 | 2.358917926 | treatment | 2.3135 | 0.020412 |
Thymol | 6.31863132 | 8.369650429 | treatment | 0.40556 | 0.022184 |
Furanodiene | 0.490262662 | 2.020872956 | treatment | 2.0434 | 0.023776 |
Deoxycytidine | 0.066672463 | 0.44656114 | treatment | 2.7437 | 0.023786 |
N-(9-oxodecyl)acetamide | 0.406044805 | 2.457205609 | treatment | 2.5973 | 0.024876 |
N’-[6-(tert-butyl)thieno [3,2-d]pyrimidin-4-yl]-4-methylbenzohydrazide | 0.401850317 | 2.668319076 | treatment | 2.7312 | 0.024881 |
trans-Cinnamic acid | 6.287254185 | 28.57467445 | treatment | 2.1842 | 0.026732 |
2-hydroxy-3,6-diphenylcyclohexyl acetate | 0.222639563 | 0.952058363 | treatment | 2.0963 | 0.027331 |
Quillaic acid | 1.204269395 | 5.036769436 | treatment | 2.0643 | 0.030163 |
Echinocystic acid | 0.638495997 | 2.319019362 | treatment | 1.8608 | 0.030859 |
Denin | 2.605601045 | 0.100645612 | control | −4.6943 | 0.030874 |
Peonidin chloride | 0.223573949 | 0.885680407 | treatment | 1.986 | 0.031339 |
Yamogenin | 0.062986529 | 0.266231264 | treatment | 2.0796 | 0.032182 |
Madecassic acid | 0.055087174 | 0.220479365 | treatment | 2.0009 | 0.032955 |
Geranylgeraniol | 0.291981112 | 0.062638856 | control | −2.2207 | 0.033176 |
2′-Deoxyadenosine | 7.18814738 | 28.88530241 | treatment | 2.0066 | 0.033775 |
1-acetyl-N-(6-chloro-1,3-benzothiazol-2-yl)-4-piperidinecarboxamide | 0.480568831 | 0.127523038 | control | −1.914 | 0.034298 |
N4-Acetylsulfamethoxazole | 2.861043764 | 0.368191965 | control | −2.958 | 0.034881 |
Umbelliferone | 1.235971892 | 0.311934508 | control | −1.9863 | 0.035234 |
Propionylcarnitine | 0.398481456 | 2.614906537 | treatment | 2.7142 | 0.035475 |
Ginsenoside-Ro | 0.04599296 | 0.015483668 | control | −1.5707 | 0.036032 |
Bornyl acetate | 3.654754691 | 11.58644708 | treatment | 1.6646 | 0.036208 |
6-Phosphogluconic acid | 10.97858566 | 2.952990938 | control | −1.8944 | 0.036683 |
Thymidine | 3.442319904 | 14.61293082 | treatment | 2.0858 | 0.037049 |
Pectolinarin | 0.312824861 | 0.058819418 | control | −2.411 | 0.03862 |
Indole-3-pyruvate | 0.005984439 | 0.029613179 | treatment | 2.307 | 0.038944 |
Phytolaccagenin | 0.157940088 | 0.64478966 | treatment | 2.0295 | 0.039018 |
Isopimpinellin | 3.939164443 | 0.119320866 | control | −5.045 | 0.040097 |
Xanthine | 6.454784926 | 26.49281664 | treatment | 2.0372 | 0.040905 |
AKBA | 0.183028523 | 0.740192089 | treatment | 2.0158 | 0.042246 |
Schisantherin E | 27.36728187 | 1.54371722 | control | −4.148 | 0.046453 |
Hypoxanthine | 19.53201248 | 134.6580964 | treatment | 2.7854 | 0.047824 |
8-iso Prostaglandin A2 | 0.411222628 | 13.63770527 | treatment | 5.0515 | 0.049548 |
N2-(6-ethoxy-1,3-benzothiazol-2-yl)-5-nitro-2-furamide | 2.635773624 | 0.681659989 | control | −1.9511 | 0.050529 |
Flavin adenine dinucleotide | 0.539526786 | 0.107283214 | control | −2.3303 | 0.051897 |
Wulignan A1 | 0.999546687 | 0.295952156 | control | −1.7559 | 0.052689 |
Avocadyne 1-acetate | 1.028969986 | 7.377756165 | treatment | 2.842 | 0.053599 |
Bevirimat | 2.046955395 | 8.851003111 | treatment | 2.1124 | 0.054015 |
Carnosic acid | 0.174778168 | 0.589385684 | treatment | 1.7537 | 0.055867 |
TPH | 1.445522233 | 0.226635062 | control | −2.6731 | 0.057537 |
4-{3-[(3,4-dihydroxyphenyl)methyl]-2-methylbutyl}benzene-1,2-diol | 1.186641805 | 0.136122491 | control | −3.1239 | 0.059361 |
KKK | 0.061126885 | 0.23307464 | treatment | 1.9309 | 0.059737 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, H.; Liang, Q.; Chen, J.; Wang, J.; Huang, Y.; Liu, B.; Zhang, X.; Zhou, B. Defense Responses in Prickly Pear (Cucumis metuliferus) to Meloidogyne incognita: Insights from Transcriptomics and Metabolomics Analysis. Agronomy 2025, 15, 1965. https://doi.org/10.3390/agronomy15081965
Zhang H, Liang Q, Chen J, Wang J, Huang Y, Liu B, Zhang X, Zhou B. Defense Responses in Prickly Pear (Cucumis metuliferus) to Meloidogyne incognita: Insights from Transcriptomics and Metabolomics Analysis. Agronomy. 2025; 15(8):1965. https://doi.org/10.3390/agronomy15081965
Chicago/Turabian StyleZhang, Hao, Qigan Liang, Jihao Chen, Jiming Wang, Yuan Huang, Bin Liu, Xuejun Zhang, and Bo Zhou. 2025. "Defense Responses in Prickly Pear (Cucumis metuliferus) to Meloidogyne incognita: Insights from Transcriptomics and Metabolomics Analysis" Agronomy 15, no. 8: 1965. https://doi.org/10.3390/agronomy15081965
APA StyleZhang, H., Liang, Q., Chen, J., Wang, J., Huang, Y., Liu, B., Zhang, X., & Zhou, B. (2025). Defense Responses in Prickly Pear (Cucumis metuliferus) to Meloidogyne incognita: Insights from Transcriptomics and Metabolomics Analysis. Agronomy, 15(8), 1965. https://doi.org/10.3390/agronomy15081965