Transcriptome analysis of a nematode resistant and susceptible upland cotton line at two critical stages of Meloidogyne incognita infection and development

English version

Autoři: Pawan Kumar ^aff001; Sameer Khanal ^aff001; Mychele Da Silva ^aff002; Rippy Singh ^aff001; Richard F. Davis ^aff002; Robert L. Nichols ^aff004; Peng W. Chee ^aff001
Působiště autorů: Dept. of Crop and Soil Sciences and Institute of Plant Breeding, Genetics, and Genomics, University of Georgia, Tifton, GA, United States of America ^aff001; Department of Plant Pathology, University of Georgia, Tifton, GA, United States of America ^aff002; USDA-ARS, Crop Protection and Management Research Unit, Tifton, GA, United States of America ^aff003; Cotton Incorporated, Cary, NC, United States of America ^aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221328

Souhrn

Host plant resistance is the most practical approach to control the Southern root-knot nematode (Meloidogyne incognita; RKN), which has emerged as one of the most serious economic pests of Upland cotton (Gossypium hirsutum L.). Previous QTL analyses have identified a resistance locus on chromosome 11 (qMi-C11) affecting galling and another locus on chromosome-14 (qMi-C14) affecting egg production. Although these two QTL regions were fine mapped and candidate genes identified, expression profiling of genes would assist in further narrowing the list of candidate genes in the QTL regions. We applied the comparative transcriptomic approach to compare expression profiles of genes between RKN susceptible and resistance genotypes at an early stage of RKN development that coincides with the establishment of a feeding site and at the late stage of RKN development that coincides with RKN egg production. Sequencing of cDNA libraries produced over 315 million reads of which 240 million reads (76%) were mapped on to the Gossypium hirsutum genome. A total of 3,789 differentially expressed genes (DEGs) were identified which were further grouped into four clusters based on their expression profiles. A large number of DEGs were found to be down regulated in the susceptible genotype at the late stage of RKN development whereas several genes were up regulated in the resistant genotype. Key enriched categories included transcription factor activity, defense response, response to phyto-hormones, cell wall organization, and protein serine/threonine kinase activity. Our results also show that the DEGs in the resistant genotype at qMi-C11 and qMi-C14 loci displayed higher expression of defense response, detoxification and callose deposition genes, than the DEGs in the susceptible genotype.

Klíčová slova:

Biology and life sciences – Genetics – Gene expression – Gene regulation – Genetic loci – Quantitative trait loci – Genomics – Genome analysis – Transcriptome analysis – Biochemistry – Proteins – DNA-binding proteins – Transcription factors – Regulatory proteins – Organisms – Eukaryota – Plants – Flowering plants – Cotton – Computational biology – Medicine and health sciences – Parasitic diseases – Nematode infections

Zdroje

1. Jones JD, Dangl JL. The plant immune system. Nature. 2006;444(7117):323–9. doi: 10.1038/nature05286 17108957

2. Shepherd RL. Transgressive Segregation for Root-Knot Nematode Resistance in Cotton. Crop Sci. 1974;14(6):872–5.

3. Jenkins JN, Creech RG, Tang B, Lawrence GW, Mccarty JC. Cotton Resistance to Root-Knot Nematode .2. Post-Penetration Development. Crop Sci. 1995;35(2):369–73.

4. Gutierrez OA, Robinson AF, Jenkins JN, McCarty JC, Wubben MJ, Callahan FE, et al. Identification of QTL regions and SSR markers associated with resistance to reniform nematode in Gossypium barbadense L. accession GB713. Theor Appl Genet. 2011;122(2):271–80. doi: 10.1007/s00122-010-1442-2 20845024

5. He YJ, Kumar P, Shen XL, Davis RF, Van Becelaere G, May OL, et al. Re-evaluation of the inheritance for root-knot nematode resistance in the Upland cotton germplasm line M-120 RNR revealed two epistatic QTLs conferring resistance. Theor Appl Genet. 2014;127(6):1343–51. doi: 10.1007/s00122-014-2302-2 24728014

6. Shen XL, Van Becelaere G, Kumar P, Davis RF, May OL, Chee P. QTL mapping for resistance to root-knot nematodes in the M-120 RNR Upland cotton line (Gossypium hirsutum L.) of the Auburn 623 RNR source. Theor Appl Genet. 2006;113(8):1539–49. doi: 10.1007/s00122-006-0401-4 16960714

7. Kumar P, He YJ, Singh R, Davis RF, Guo H, Paterson AH, et al. Fine mapping and identification of candidate genes for a QTL affecting Meloidogyne incognita reproduction in Upland cotton. Bmc Genomics. 2016;17. doi: 10.1186/s12864-015-2333-3

8. Andrews S. FastQC: a quality control tool for high throughput sequence data. 2010.

9. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404

10. Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature biotechnology. 2015;33(5):531–7. doi: 10.1038/nbt.3207 25893781

11. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nature protocols. 2016;11(9):1650–67. doi: 10.1038/nprot.2016.095 27560171

12. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8 25516281

13. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA. Primer3Plus, an enhanced web interface to Primer3. Nucleic acids research. 2007;35(Web Server issue), W71–W74. doi: 10.1093/nar/gkm306 17485472

14. Zhao S, Fernald, RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of computational biology: a journal of computational molecular cell biology. 2005;12(8), 1047–1064. doi: 10.1089/cmb.2005.12.1047 16241897

15. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic acids research; 2002; 30(9), e36. doi: 10.1093/nar/30.9.e36 11972351

16. Licausi F, Ohme‐Takagi M, Perata PJNP. APETALA 2/Ethylene Responsive Factor (AP 2/ERF) transcription factors: mediators of stress responses and developmental programs. 2013;199(3):639–49.

17. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder JJMP-MI. Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. 2000;13(10):1121–9. doi: 10.1094/MPMI.2000.13.10.1121 11043473

18. Grunewald W, Van Noorden G, Van Isterdael G, Beeckman T, Gheysen G, Mathesius UJTPC. Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. 2009;21(9):2553–62. doi: 10.1105/tpc.109.069617 19789282

19. Goverse A, Bird D. The role of plant hormones in nematode feeding cell formation. Genomics and Molecular Genetics of Plant-Nematode Interactions: Springer; 2011. p. 325–47.

20. Dowd CD, Chronis D, Radakovic ZS, Siddique S, Schmülling T, Werner T, et al. Divergent expression of cytokinin biosynthesis, signaling and catabolism genes underlying differences in feeding sites induced by cyst and root‐knot nematodes. The Plant Journal. 2017.

21. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J. Nematode feeding sites: unique organs in plant roots. Planta. 2013;238(5):807–18. doi: 10.1007/s00425-013-1923-z 23824525

22. Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, et al. Expansins are involved in the formation of nematode‐induced syncytia in roots of Arabidopsis thaliana. The Plant Journal. 2006;48(1):98–112. doi: 10.1111/j.1365-313X.2006.02856.x 16942607

23. Wieczorek K, Hofmann J, Blöchl A, Szakasits D, Bohlmann H, Grundler FM. Arabidopsis endo‐1, 4‐β‐glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. The Plant Journal. 2008;53(2):336–51. doi: 10.1111/j.1365-313X.2007.03340.x 18069944

24. Scheller HV, Ulvskov P. Hemicelluloses. Annual review of plant biology. 2010;61.

25. Nishitani K, Vissenberg K. Roles of the XTH protein family in the expanding cell. The expanding cell: Springer; 2006. p. 89–116.

26. Wuyts N, Lognay G, Swennen R, De Waele DJJoeb. Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. 2006;57(11):2825–35.

27. Wuyts N, Lognay G, Verscheure M, Marlier M, De Waele D, Swennen RJPp. Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). 2007;56(5):878–90.

28. Kumari C, Dutta TK, Banakar P, Rao UJSr. Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice. 2016;6:22846.

29. Zhang SH, Yang Q, Ma RCJJoIPB. Erwinia carotovora ssp. carotovora infection induced “defense lignin” accumulation and lignin biosynthetic gene expression in Chinese cabbage (Brassica rapa L. ssp. pekinensis). 2007;49(7):993–1002.

30. Ma Q-H, Zhu H-H, Han J-QJPS. Wheat ROP proteins modulate defense response through lignin metabolism. 2017;262:32–8.

31. Wang G-F, He Y, Strauch R, Olukolu BA, Nielsen D, Li X, et al. Maize homologs of hydroxycinnamoyltransferase, a key enzyme in lignin biosynthesis, bind the nucleotide binding leucine-rich repeat Rp1 proteins to modulate the defense response. 2015;169(3):2230–43.

32. Ruben E, Jamai A, Afzal J, Njiti V, Triwitayakorn K, Iqbal M, et al. Genomic analysis of the rhg1 locus: candidate genes that underlie soybean resistance to the cyst nematode. Molecular Genetics and Genomics. 2006;276(6):503–16. doi: 10.1007/s00438-006-0150-8 17024428

33. Afzal AJ, Natarajan A, Saini N, Iqbal MJ, Geisler M, El Shemy HA, et al. The nematode resistance allele at the rhg1 locus alters the proteome and primary metabolism of soybean roots. Plant physiology. 2009;151(3):1264–80. doi: 10.1104/pp.109.138149 19429603

34. Sekhwal MK, Li P, Lam I, Wang X, Cloutier S, You FMJIJoMS. Disease resistance gene analogs (RGAs) in plants. 2015;16(8):19248–90.

35. Fodor J, Gullner G, Ádám AL, Barna B, Komives T, Király ZJPP. Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco (role in systemic acquired resistance). 1997;114(4):1443–51.

36. Herbette S, Lenne C, De Labrouhe DT, Drevet JR, Roeckel‐Drevet PJPP. Transcripts of sunflower antioxidant scavengers of the SOD and GPX families accumulate differentially in response to downy mildew infection, phytohormones, reactive oxygen species, nitric oxide, protein kinase and phosphatase inhibitors. 2003;119(3):418–28.

37. Wubben MJ, Callahan FE, Jenkins JN, Deng DDJT, genetics a. Coupling of MIC-3 overexpression with the chromosomes 11 and 14 root-knot nematode (RKN)(Meloidogyne incognita) resistance QTLs provides insights into the regulation of the RKN resistance response in Upland cotton (Gossypium hirsutum). 2016;129(9):1759–67.

38. Wubben MJ TG, Lee P, Callahan FE, Deng DD, McCarty JC, Jenkins JN. Marker-assisted-selection coupled with recombinant inbred line genome sequencing identifies a root-knot nematode resistance gene on chromosome 14 in upland cotton. Annual meeting, society of nematologists; July 22–25; Albuquerque, New Mexico, USA2018.

Transcriptome analysis of a nematode resistant and susceptible upland cotton line at two critical stages of Meloidogyne incognita infection and development

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz