Molecular and Functional Characterization of Chemosensory Genes from the Root-knot Nematode Meloidogyne Graminicola

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2023 Dec 6

PMID 38057766

Authors

Tushar K Dutta

Voodikala S Akhil

Manoranjan Dash

Artha Kundu

Victor Phani

Anil Sirohi

Affiliations

Soon will be listed here.

Abstract

Background: Root-knot nematode Meloidogyne graminicola has emerged as a major threat in rice agroecosystems owing to climate change-induced changes in cultivation practices. Synthetic nematicides are continually being withdrawn from the nematode management toolbox because of their ill effects on the environment. A sustainable strategy would be to develop novel nematicides or resistant plants that would target nematode sensory perception, which is a key step in the host finding biology of plant-parasitic nematodes (PPNs). However, compared to the extensive literature on the free-living nematode Caenorhabditis elegans, negligible research has been performed on PPN chemosensory biology.

Results: The present study characterizes the five chemosensory genes (Mg-odr-7, Mg-tax-4, Mg-tax-4.1, Mg-osm-9, and Mg-ocr-2) from M. graminicola that are putatively associated with nematode host-finding biology. All the genes were highly transcribed in the early life stages, and RNA interference (RNAi)-induced downregulation of each candidate gene perturbed the normal behavioural phenotypes of M. graminicola, as determined by examining the tracking pattern of juveniles on Pluronic gel medium, attraction to and penetration in rice root tip, and developmental progression in rice root. In addition, a detrimental effect on nematode chemotaxis towards different volatile and nonvolatile organic compounds and host root exudates was documented.

Conclusion: Our findings enrich the existing literature on PPN chemosensory biology and can supplement future research aimed at identifying a comprehensive chemosensory signal transduction pathway in PPNs.

Citing Articles

Induced knockdown of and perturbed the host seeking behavior of in rice.

Dutta T, Akhil V, Kundu A, Dash M, Phani V, Sirohi A Heliyon. 2024; 10(4):e26384.

PMID: 38420492 PMC: 10900406. DOI: 10.1016/j.heliyon.2024.e26384.

References

Dutta T, Banakar P, Rao U . The status of RNAi-based transgenic research in plant nematology. Front Microbiol. 2015; 5:760. PMC: 4290618. DOI: 10.3389/fmicb.2014.00760. View

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. DOI: 10.1016/j.pbi.2019.02.007. View

Teillet A, Dybal K, Kerry B, Miller A, Curtis R, Hedden P . Transcriptional changes of the root-knot nematode Meloidogyne incognita in response to Arabidopsis thaliana root signals. PLoS One. 2013; 8(4):e61259. PMC: 3625231. DOI: 10.1371/journal.pone.0061259. View

Yan Y, Davis E . Characterisation of guanylyl cyclase genes in the soybean cyst nematode, Heterodera glycines. Int J Parasitol. 2002; 32(1):65-72. DOI: 10.1016/s0020-7519(01)00315-0. View

SENGUPTA P, Colbert H, Bargmann C . The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell. 1994; 79(6):971-80. DOI: 10.1016/0092-8674(94)90028-0. View

Kyndt T, Fernandez D, Gheysen G . Plant-parasitic nematode infections in rice: molecular and cellular insights. Annu Rev Phytopathol. 2014; 52:135-53. DOI: 10.1146/annurev-phyto-102313-050111. View

Spence K, Lewis E, Perry R . Host-finding and invasion by entomopathogenic and plant-parasitic nematodes: evaluating the ability of laboratory bioassays to predict field results. J Nematol. 2009; 40(2):93-8. PMC: 2586539. View

Kumari C, Dutta T, 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. PMC: 4785349. DOI: 10.1038/srep22846. View

OHalloran D, Altshuler-Keylin S, Zhang X, He C, Morales-Phan C, Yu Y . Contribution of the cyclic nucleotide gated channel subunit, CNG-3, to olfactory plasticity in Caenorhabditis elegans. Sci Rep. 2017; 7(1):169. PMC: 5427828. DOI: 10.1038/s41598-017-00126-7. View

10.

Rosso M, Jones J, Abad P . RNAi and functional genomics in plant parasitic nematodes. Annu Rev Phytopathol. 2009; 47:207-32. DOI: 10.1146/annurev.phyto.112408.132605. View

11.

Shivakumara T, Dutta T, Chaudhary S, Von Reuss S, Williamson V, Rao U . Homologs of Chemosensory Genes Have Roles in Behavior and Chemotaxis in the Root-Knot Nematode . Mol Plant Microbe Interact. 2019; 32(7):876-887. DOI: 10.1094/MPMI-08-18-0226-R. View

12.

Curtis R . Plant-nematode interactions: environmental signals detected by the nematode's chemosensory organs control changes in the surface cuticle and behaviour. Parasite. 2008; 15(3):310-6. DOI: 10.1051/parasite/2008153310. View

13.

Reynolds A, Dutta T, Curtis R, Powers S, Gaur H, Kerry B . Chemotaxis can take plant-parasitic nematodes to the source of a chemo-attractant via the shortest possible routes. J R Soc Interface. 2010; 8(57):568-77. PMC: 3061123. DOI: 10.1098/rsif.2010.0417. View

14.

Lilley C, Davies L, Urwin P . RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology. 2012; 139(5):630-40. DOI: 10.1017/S0031182011002071. View

15.

Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R . Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron. 2002; 35(2):307-18. DOI: 10.1016/s0896-6273(02)00757-2. View

16.

Cheng W, Xue H, Yang X, Huang D, Cai M, Huang F . Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria. Microbiol Spectr. 2022; 11(1):e0231922. PMC: 9927473. DOI: 10.1128/spectrum.02319-22. View

17.

Shuart N, Haitin Y, Camp S, Black K, Zagotta W . Molecular mechanism for 3:1 subunit stoichiometry of rod cyclic nucleotide-gated ion channels. Nat Commun. 2011; 2:457. PMC: 3265371. DOI: 10.1038/ncomms1466. View

18.

Kikuchi T, Eves-van den Akker S, Jones J . Genome Evolution of Plant-Parasitic Nematodes. Annu Rev Phytopathol. 2017; 55:333-354. DOI: 10.1146/annurev-phyto-080516-035434. View

19.

Wubben 2nd M, Su H, Rodermel S, Baum T . Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol Plant Microbe Interact. 2001; 14(10):1206-12. DOI: 10.1094/MPMI.2001.14.10.1206. View

20.

Fukagawa N, Ziska L . Rice: Importance for Global Nutrition. J Nutr Sci Vitaminol (Tokyo). 2019; 65(Supplement):S2-S3. DOI: 10.3177/jnsv.65.S2. View