Skip to main content
Log in

Marker-assisted selection in Gossypium spp. for Meloidogyne incognita resistance and histopathological characterization of a near immune line

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

The root-knot nematode, Meloidogyne incognita, is one of the most important parasites that cause economic losses in the cotton crop. Plant genetic resistance is the most desirable strategy to control this pathogen. Sources of resistance in cotton have been known for several years but only a few resistant commercial varieties have been released. Cotton breeding lines were developed using marker-assisted selection in early generation plants to introgress root-knot resistance genes from two different sources: M-315 or CIR1348. Phenotyping was carried out in greenhouse conditions to validate the molecular markers associated with the resistance genes in the breeding lines and confirmed by genotyping. The markers targeting QTLs from M-315 resistance source were highly efficient in the selection of plants resistant to M. incognita, with all plants expressing a reproduction factor inferior to 0.08. CIR1348 resistance source markers were also very efficient in selecting resistance; however, some segregation events revealed the need for fine mapping of the resistance QTLs. To clarify the resistance mechanisms, present in the germplasm derived from the M-315 resistance source, the resistant line CNPA 17-26 B2RF (triple cross [BRS 368RF × M-315] × [BRS 430B2RF]) was chosen for histopathological characterization of plant-nematode interaction and compared with the susceptible FiberMax 966 (FM 966). The second-stage juveniles (J2) penetrated equally in both genotypes. In the histopathological study, a strong blue fluorescence was visualized in the tissues around the nematode (hypersensitivity reaction, HR), mainly at the beginning (from 2 to 6 DAI) in the cortex and central cylinder of the resistant plant, indicating accumulation of phenolic compounds in the roots. At 9 DAI, giant cells in the early stage of subdivision next to nematodes were observed in the central cylinder of the resistant plant, and phenolic compounds were also shown around the nematode. At 12–40 DAI these initial cells were completely degraded with the presence of phenolics involving the nematodes and initial giant cells. No fully developed giant cells or mature females were observed, only fourth-stage juveniles (J4s), and males were frequently visualized at 34 DAI. This resistance mechanism characterizes near-immunity, and so no enlarged females and no egg production were observed. In susceptible control, it was possible to visualize feeding sites well developed from 6 to 30 DAI. Females reached maturity at 26 DAI, and eggs were observed at 30 DAI. Our results suggested that the resistance (near-immunity) of the line CNPA 17-26 B2RF was related to early (2–12 DAI) defense responses that totally prevented nematode reproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • ABRAPA (2017) Associação Brasileira dos Produtores de Algodão. Accessed 23 Sept 2018

  • Anwar SA, McKenry MV (2002) Penetration and development of Meloidogyne arenaria on two new grape rootstocks. J Nematol 34:143–145

    PubMed  PubMed Central  Google Scholar 

  • Barroso PAV, Suassuna ND, Pedrosa MB, Morello CL, Filho JLS, Lamas FM, Bogiani JC (2017) BRS 368RF: A glyphosate tolerant, midseason upland cotton cultivar for Northeast and North Brazilian cerrado. Crop Breed Appl Biotechnol 17(4):399–402

    CAS  Google Scholar 

  • Bendezu IF, Starr JL (2003) Mechanism of resistance to Meloidogyne arenaria in the peanut cultivar COAN. J Nematol 35:115–118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Byrd DW, Kirkpatrick T, Barker KR (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15:142–143

    Google Scholar 

  • Creech RG, Jenkins JN, Tang B, Lawrence GW, McCarty JC (1995) Cotton resistance to root-knot nematode: I. Penetration and reproduction. Crop Sci 35:365–368

    Google Scholar 

  • de Carvalho LP, Farias FJC, Rodrigues JIS, Suassuna ND, Teodoro PE (2017) Genetic diversity among exotic cotton accessions as for qualitative and quantitative traits. Genet Mol Res. https://doi.org/10.4238/gmr16019590

    Article  PubMed  Google Scholar 

  • Fang DD, Xiao J, Canci PC, Cantrell RG (2010) A new SNP haplotype associated with blue disease resistance gene in cotton (Gossypium hirsutum L.). Theor Appl Genet 120:943–953

    CAS  PubMed  Google Scholar 

  • Fassuliotis G (1970) Resistance of Cucumis spp. to the root-knot nematode, Meloidogyne incognita acrita. J Nematol 2:174–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freitas VM, Correia VR, Motta FC, Sousa MG, Gomes ACMM, Carneiro MDG, Silva DB, Mattos JK, Nicole M, Carneiro RMDG (2014) Resistant accessions of wild Psidium spp. to Meloidogyne enterolobii and histological characterization of resistance. Plant Pathol 63:738–746

    Google Scholar 

  • Galbieri R, Asmus GL (2016) Principais espécies de nematoides do algodoeiro no Brasil. In: Galbieri R, Belot JL (eds) Nematoides fitoparasitas do algodoeiro nos cerrados brasileiros: biologia e medidas de controle. IMAmt, Cuiabá, pp 11–36

    Google Scholar 

  • Galbieri R, Belot JL, Vilela PA, Cia E (2019) Avaliação da resistência e da tolerância de cultivares de algodoeiro ao nematoide-das-galhas. Instituto Matogrossense do Algodão 42:1–8

    Google Scholar 

  • Gomes GM, Moretzsohn MC, Da Silva EH, Furlanetto C, Silva JGP, Lacape JM, Barroso PAV, Carneiro RMDG, Giband M (2016) Mapping of QTLs identified in a novel source of resistance to the root-knot nematode (Meloidogyne incognita race 3) in cotton (Gossypium barbadense L.). In: ICAC (ed) World cotton research conference, Goiânia, Brazil 2016, pp 163–164

  • Gutiérrez OA, Stelly DM, Saha S, Jenkins JN, McCarty JC, Raska DA, Scheffler BE (2010) SSR markers closely associated with genes for resistance to root- knot nematode on chromosomes 11 and 14 of Upland cotton. Theor Appl Genet 121:1323–1337

    PubMed  Google Scholar 

  • Hartman KM, Sasser JN (1985) Identification of Meloidogyne species on the basis of differential host test and perineal pattern morphology. In: Carter CC, Sasser JN (eds) An advanced treatise on Meloidogyne, vol II. Methodology. North Carolina State University Graphics, Raleigh, pp 69–77

    Google Scholar 

  • He Y, Kumar P, Shen X, Davis RF, Van Becelaere G, May OL, Nichols RL, Chee PW (2014) 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 127:1343–1351

    CAS  PubMed  Google Scholar 

  • Hussey RS, Barker KR (1973) A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep 57:1025–1028

    Google Scholar 

  • Jenkins JN (2003) Cotton. In: OECD (ed) Traditional crop breeding practices: an historical review to serve as a baseline for assessing the role of modern biotechnology. Organization for Economic Co-Operation and Development (OECD), Paris, pp 61–70

    Google Scholar 

  • Jenkins JN, Creech RG, Tang B, Lawrence GW, McCarty JC (1995) Cotton resistance to root-knot nematode: II. Post-penetration development. Crop Sci 35:369–373

    Google Scholar 

  • Jenkins JN, McCarty JC, Wubben MJ, Hayes R, Gutierrez OA, Callahan F, Deng D (2012) SSR markers for marker assisted selection of root-knot nematode (Meloidogyne incognita) resistant plants in cotton (Gossypium hirsutum L). Euphytica 183:49–54

    CAS  Google Scholar 

  • Lima EA, Furlanetto C, Nicole M, Gomes ACMM, Almeida MRA, Jorge-Junior A, Correa VR, Salgado SML, Ferrão MA, Carneiro RMDG (2015) The multi-resistant reaction of drought-tolerant coffee Conilon clone 14 to Meloidogyne spp. and late hypersensitive-like response in Coffea canephora. Phytopathology 105:805–814

    PubMed  Google Scholar 

  • Lopes CML, Cares JE, Perina FJ, Nascimento GF, Mendonça JSF, Moita AW, Castagnone-Sereno P, Carneiro RMDG (2019) Diversity of Meloidogyne incognita populations from cotton and aggressiveness to Gossypium spp. accessions. Plant Pathol 68:816–824

    Google Scholar 

  • McCarty JC, Jenkins JN, Wubben MJ, Hayes RW, Callahan FE, Deng D (2017) Registration of six germplasm lines of cotton with resistance to the root-knot and reniform nematodes. J Plant Regist 11:168–171

    Google Scholar 

  • McPherson MG, Jenkins JN, Watson CE, McCarty JC (2004) Inheritance of root-knot nematode resistance in M-315 RNR and M-78 RNR cotton. J Cotton Sci 8:154–161

    Google Scholar 

  • Menezes IPP, Gaiotto FA, Suassuna ND, Hoffmann LV, Barroso PAV (2014) Susceptibility of Gossypium mustelinum populations to the main cotton diseases in Brazil. J Agric Sci 6:39–47

    Google Scholar 

  • Mota FC, Alves GCS, Giband M, Gomes ACMM, Sousa FR, Mattos VS, Barbosa VHS, Barroso PAV, Michel N, Peixoto JR, Rocha MR, Carneiro RMDG (2012) New sources of resistance to Meloidogyne incognita race 3 in wild cotton accessions and histological characterization of the defense mechanisms. Plant Pathol 62:1173–1183

    Google Scholar 

  • Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:369–389

    CAS  Google Scholar 

  • Pegard A, Brizzard G, Fazari A, Soucaze O, Abad P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology 95:158–165

    CAS  PubMed  Google Scholar 

  • Pofu KM, Mashela PW (2011) Using relative penetration and maleness indices in Meloidogyne incognita to establish resistance type in Cucumis myriocarpus. Afr J Biotechnol 10:390–393

    Google Scholar 

  • Proite K, Carneiro R, Falcão R, Gomes A, Leal-Bertioli S, Guimarães P, Bertioli D (2008) Post-infection development and histopathology of Meloidogyne arenaria race 1 on Arachis spp. Plant Pathol 57:974–980

    Google Scholar 

  • Robinson AF (2008) Nematode management in cotton. In: Ciancio A, Mukerji KG (eds) Integrated management of biocontrol of vegetable and grain crops nematodes. Springer, New York, pp 149–182

    Google Scholar 

  • Shen X, Van Becelaere G, Kumar P, Davis RF, Chee PW (2006) 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 113:1539–1549

    CAS  PubMed  Google Scholar 

  • Shen X, He Y, Lubbers EL, Davis RF, Nichols RL, Chee PW (2010) Fine mapping QMi-C11 a major QTL controlling root-knot nematodes resistance in Upland cotton. Theor Appl Genet 121:1623–1631

    PubMed  Google Scholar 

  • Shepherd RL (1974) Transgressive segregation for root-knot nematode resistance in cotton. Crop Sci 14:872–875

    Google Scholar 

  • Shepherd RL (1982) Registration of 3 germplasm lines of cotton. Crop Sci 22(3):692

    Google Scholar 

  • Shepherd RL, McCarty JC, Jenkins JN, Parrott WL (1996) Registration of nine cotton germplasm lines resistant to root-knot nematode. Crop Sci 36(3):820. https://doi.org/10.2135/cropsci1996.0011183X003600030071x

    Article  Google Scholar 

  • Silva EH (2014) Variabilidade genética e fisiológica de populações de Meloidogyne incognita e identificação de QTLs de uma nova fonte de resistência do algodoeiro (Gossypium spp.) a esse nematoide. Universidade de Brasília, Brasília

    Google Scholar 

  • Silva EH, Mattos VS, Furlanetto C, Giband M, Barroso PAV, Moita AW, Jorge-Junior A, Correa VR, Castagnone-Sereno P, Carneiro RMDG (2014) Genetic variability and virulence of Meloidogyne incognita populations from Brazil to resistant cotton genotypes. Eur J Plant Pathol 139:195–204

    Google Scholar 

  • Silva MBD, Davis RF, Kumar P, Nichols RL, Chee PW (2019) Resistance QTLs qMi-C11 and qMi-C14 in cotton have different effects on the development of Meloidogyne incognita, the southern root-knot nematode. Plant Dis 103:853–858

    PubMed  Google Scholar 

  • Silva Neto SP, Pereira AF, Morello CL, Suassuna ND (2016) Melhoramento clássico e biotecnologia visando a superação de desafios. In: Piccoli GV, Dalcin E (eds) Desafios do cerrado: Como sustentar a expansão da produção com produtividade e competitiva. Associação Matogrossense dos Produtores de Algodão, Cuiabá, pp 215–253

    Google Scholar 

  • Suassuna ND, Scoz LB, Giband M (2016) Melhoramento genético do algodoeiro para resistência aos nematoides: seleção assistida por marcadores moleculares. In: Galbieri R, Belot JL (eds) Nematoides fitoparasitas do algodoeiro nos cerrados brasileiros: biologia e medidas de controle. Instituto Mato-grossense do Algodão, Cuiabá, pp 243–256

    Google Scholar 

  • Suassuna ND, Lopes CML, Perina FJ, Silva Filho JL, Morello CL, Carneiro RMDG (2019) Piramiding resistance to main cotton diseases in Brazil. In: Beltwide cotton conferences, New Orleans, MS, USA, 2019. Natl Cotton Council of America

  • Ulloa M, Wang C, Roberts PA (2010) Gene action analysis by inheritance and quantitative trait loci mapping of resistance to root-knot nematodes in cotton. Plant Breed 129:541–550

    CAS  Google Scholar 

  • Wang C, Ulloa M, Roberts PA (2006) Identification and mapping of microsatellite markers linked to a root-knot nematode resistance gene (rkn1) in AcalaNemX cotton (Gossypium hirsutum L.). Theor Appl Genet 112:770–777

    CAS  PubMed  Google Scholar 

  • Weaver DB (2015) Cotton nematodes. In: Fang DD, Percy RG (eds) Cotton. ASA, CSSA and SSSA, Madison, pp 1–24

    Google Scholar 

  • Wendel JF, Grover CE (2015) Taxonomy and evolution of the cotton genus, Gossypium. In: Fang DD, Percy RG (eds) Cotton, vol 57. American Society of Agronomy Inc., Madison, pp 25–44. https://doi.org/10.2134/agronmonogr57.2013.0020

    Chapter  Google Scholar 

  • Wendel JF, Brubaker C, Alvarez I, Cronn R, Stewart JM (2009) Evolution and natural history of the cotton genus. In: Paterson AH (ed) Genetics and genomics of cotton, plant genetics and genomics: crops and models, vol 3. Springer, New York, pp 3–22

    Google Scholar 

  • Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403

    CAS  PubMed  Google Scholar 

  • Wu Z, Solimar KM, Zipf A, Saha S, Sharma GC, Jenkins JN (2005) Isolation and characterization of genes differentially expressed in fiber of Gossypium barbadense L. J Cotton Sci 9:166–174

    CAS  Google Scholar 

  • Xiao J, Fang DD, Bhatti M, Hendrix B, Cantrell RG (2010) A SNP haplotype associated with a gene resistant to Xanthomonas axonopodis pv. malvacearum in upland cotton (Gossypium hirsutum L.). Mol Breed 25:593–602

    CAS  Google Scholar 

  • Ynturi P, McCarty JC, Gutierrez OA, Saha S (2006) Association of root-knot nematode resistance genes with simple sequence repeat markers on two chromosomes in cotton. Crop Sci 46:2670–2674

    CAS  Google Scholar 

  • Yuksel B, Khezir H, Adem B, Muhammad TA (2016) Insight in the utilization of marker assisted selection in cotton. Mol Plant Breed 7:1–17

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. M. L. Lopes.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lopes, C.M.L., Suassuna, N.D., Cares, J.E. et al. Marker-assisted selection in Gossypium spp. for Meloidogyne incognita resistance and histopathological characterization of a near immune line. Euphytica 216, 19 (2020). https://doi.org/10.1007/s10681-020-2554-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-020-2554-7

Keywords

Navigation