The heterologous expression of conserved Glycine max (soybean) mitogen activated protein kinase 3 (MAPK3) paralogs suppresses Meloidogyne incognita parasitism in Gossypium hirsutum (upland cotton)

Vincent P Klink; Nadim W Alkharouf; Kathy S Lawrence; Bisho R Lawaju; Keshav Sharma; Prakash M Niraula; Brant T McNeece

doi:10.1007/s11248-022-00312-y

The heterologous expression of conserved Glycine max (soybean) mitogen activated protein kinase 3 (MAPK3) paralogs suppresses Meloidogyne incognita parasitism in Gossypium hirsutum (upland cotton)

Transgenic Res. 2022 Oct;31(4-5):457-487. doi: 10.1007/s11248-022-00312-y. Epub 2022 Jun 28.

Authors

Vincent P Klink^{1

2

3}, Nadim W Alkharouf⁴, Kathy S Lawrence^{5

6}, Bisho R Lawaju^{5

7

8}, Keshav Sharma^{9

7

10}, Prakash M Niraula^{9

7

11}, Brant T McNeece^{9

7

12}

Affiliations

¹ USDA ARS NEA BARC Molecular Plant Pathology Laboratory, Building 004 Room 122 BARC-West, 10300 Baltimore Ave., Beltsville, MD, 20705, USA. vincent.klink@usda.gov.
² Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, 39762, USA. vincent.klink@usda.gov.
³ Center for Computational Sciences High Performance Computing Collaboratory, Mississippi State University, Mississippi State, MS, 39762, USA. vincent.klink@usda.gov.
⁴ Department of Computer and Information Sciences, Towson University, Towson, MD, 21252, USA.
⁵ Department of Entomology and Plant Pathology, Auburn University, 209 Life Science Building, Auburn, AL, 36849, USA.
⁶ Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Auburn University, 209 Life Science Building, Auburn, AL, 36849, USA.
⁷ Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, 39762, USA.
⁸ Department of Plant Pathology, North Dakota State University, 1402 Albrecht Blvd., Walster Hall 306, Fargo, ND, 58102, USA.
⁹ Department of Biological Sciences, Mississippi State University, Mississippi State, MS, 39762, USA.
¹⁰ Cereal Disease Laboratory, 1551 Lindig Street, Saint Paul, MN, 55108, USA.
¹¹ Department of Biological Sciences, Delaware State University, 1200 North Dupont Highway, Science Center 164, Dover, DE, 19901, USA.
¹² Nutrien Ag Solutions, 737 Blaylock Road, Winterville, MS, 38703, USA.

Abstract

Two conserved Glycine max (soybean) mitogen activated protein kinase 3 (MAPK3) paralogs function in defense to the parasitic soybean cyst nematode Heterodera glycines. Gene Ontology analyses of RNA seq data obtained from MAPK3-1-overexpressing (OE) and MAPK3-2-OE roots compared to their control, as well as MAPK3-1-RNA interference (RNAi) and MAPK3-2-RNAi compared to their control, hierarchically orders the induced and suppressed genes, strengthening the hypothesis that their heterologous expression in Gossypium hirsutum (upland cotton) would impair parasitism by the root knot nematode (RKN) Meloidogyne incognita. MAPK3-1 expression (E) in G. hirsutum suppresses the production of M. incognita root galls, egg masses, and second stage juveniles (J2s) by 80.32%, 82.37%, and 88.21%, respectfully. Unexpectedly, egg number increases by 28.99% but J2s are inviable. MAPK3-2-E effects are identical, statistically. MAPK3-1-E and MAPK3-2-E decreases root mass 1.49-fold and 1.55-fold, respectively, as compared to the pRAP15-ccdB-E control. The reproductive factor (RF) of M. incognita for G. hirsutum roots expressing MAPK3-1-E or MAPK3-2-E decreases 60.39% and 50.46%, respectively, compared to controls. The results are consistent with upstream pathogen activated molecular pattern (PAMP) triggered immunity (PTI) and effector triggered immunity (ETI) functioning in defense to H. glycines. The experiments showcase the feasibility of employing MAPK3, through heterologous expression, to combat M. incognita parasitism, possibly overcoming impediments otherwise making G. hirsutum's defense platform deficient. MAPK homologs are identified in other important crop species for future functional analyses.

Keywords: Cotton; Effector triggered immunity (ETI) pathogen associated molecular pattern (PAMP) triggered immunity (PTI); Gene Ontology; Glycine max; Gossypium hirsutum; Mitogen activated protein kinase (MAPK); Overexpression; Plant parasitic nematode; RNA interference (RNAi); Soybean.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Glycine max / parasitology
Gossypium / genetics
Mitogen-Activated Protein Kinase 3
Pathogen-Associated Molecular Pattern Molecules
Plant Diseases / parasitology
Tylenchoidea* / genetics

Substances

Pathogen-Associated Molecular Pattern Molecules
Mitogen-Activated Protein Kinase 3