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Inheritance and metabolomics of the resistance of two F2 populations of Phaseolus spp. to Acanthoscelides obtectus

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Abstract

The bean weevil Acanthoscelides obtectus is one of the major storage pests of dry bean. Tepary bean (Phaseolus acutifolius) is a great source of resistance against A. obtectus to improve dry bean production. We developed two F2 populations of Phaseolus spp. by crossing bean genotypes resistant to A. obtectus × susceptible, to (1) search for metabolites related to bean weevil resistance using an untargeted metabolomics approach and (2) understand the genetics of resistance to A. obtectus attack using the number of adults emerged from seeds as resistance criteria. The segregation of the number of adults emerged from seeds showed that the genetics of resistance (0 emerged adults = resistant, 1 or more emerged adults = susceptible) was controlled by a single dominant gene in two (resistant × susceptible) F2 populations. From nine metabolites detected, pipecolic acid concentration was significantly higher in the testa of resistant individuals than in the testa of susceptible individuals. From a breeding point of view, (P. Saltillo × T. amarillo) F2 is of special interest because it is derived from a cultivated tepary × cultivated common bean cross and showed 3:1 resistant vs susceptible segregation. Therefore, this F2 is a suitable base material for breeding programmes to obtain new bean lines with good agronomic performance, seed quality and resistance to insect attack. Pipecolic acid plays a role in resistance against A. obtectus.

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Data availability

Small quantities of seed of T. cafe, T. amarillo, and P. saltillo for research purposes are available from the corresponding author. Seeds of the populations are not available because are in F3. The datasets during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abeysekara NS, Swaminathan S, Desai N, Guo L, Bhattacharyya MK (2016) The plant immunity inducer pipecolic acid accumulates in the xylem sap and leaves of soybean seedlings following Fusarium virguliforme infection. Plant Sci 243:105–114

    CAS  PubMed  Google Scholar 

  • Akibode CS, Maredia MK (2012) Global and regional trends in production, trade and consumption of food legume crops.

  • Aranega-Bou P, de la O Leyva M, Finiti I, García-Agustín P, González-Bosch C (2014) Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci 5:488

    PubMed  PubMed Central  Google Scholar 

  • Banday ZZ, Nandi AK (2015) Interconnection between flowering time control and activation of systemic acquired resistance. Front Plant Sci 6:174

    PubMed  PubMed Central  Google Scholar 

  • Bernsdorff F, Döring A-C, Gruner K, Schuck S, Bräutigam A, Zeier J (2016) Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and-independent pathways. Plant Cell 28:102–129

    CAS  PubMed  Google Scholar 

  • Brenner SA, Romeo JT (1986) Fungitoxic effects of nonprotein imino acids on growth of saprophytic fungi isolated from the leaf surface of Calliandra haematocephala. Appl Environ Microbiol 51:690–693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardona C, Posso CE, Kornegay J, Valor J, Serrano M (1989) Antibiosis effects of wild dry bean accessions on the Mexican bean weevil and the bean weevil (Coleoptera: Bruchidae). J Econ Entomol 82:310–315

    Google Scholar 

  • Cecchini NM, Jung HW, Engle NL, Tschaplinski TJ, Greenberg JT (2015) ALD1 regulates basal immune components and early inducible defense responses in Arabidopsis. Mol Plant Microbe Interact 28:455–466. https://doi.org/10.1094/mpmi-06-14-0187-r

    Article  CAS  PubMed  Google Scholar 

  • Chen Y-C, Holmes EC, Rajniak J, Kim J-G, Tang S, Fischer CR, Mudgett MB, Sattely ES (2018) N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. Proc Natl Acad Sci 115:E4920–E4929

    CAS  PubMed  Google Scholar 

  • Ding P, Rekhter D, Ding Y, Feussner K, Busta L, Haroth S, Xu S, Li X, Jetter R, Feussner I (2016) Characterization of a pipecolic acid biosynthesis pathway required for systemic acquired resistance. Plant Cell 28:2603–2615

    CAS  PubMed  PubMed Central  Google Scholar 

  • Donze-Reiner T, Palmer NA, Scully ED, Prochaska TJ, Koch KG, Heng-Moss T, Bradshaw JD, Twigg P, Amundsen K, Sattler SE, Sarath G (2017) Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs. BMC Plant Biol 17:46. https://doi.org/10.1186/s12870-017-0998-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonçalves GLP, Ribeiro L.d.P., Gimenes L., Vieira P.C., Silva M.F.d.G.F.d., Forim M.R., Fernandes J.B., Vendramim J.D. (2015) Lethal and sublethal toxicities of Annona sylvatica (Magnoliales: Annonaceae) Extracts to Zabrotes subfasciatus (Coleoptera: Chrysomelidae: Bruchinae). Florida Entomol 98:921–928. https://doi.org/10.1653/024.098.0317

    Article  Google Scholar 

  • Gruner K, Griebel T, Návarová H, Attaran E, Zeier J (2013) Reprogramming of plants during systemic acquired resistance. Front Plant Sci 4:252

    PubMed  PubMed Central  Google Scholar 

  • Guerra T, Schilling S, Hake K, Gorzolka K, Sylvester FP, Conrads B, Westermann B, Romeis T (2019) Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐l‐pipecolic acid‐and SARD 1‐dependent immune memory in systemic acquired resistance. New Phytologist.

  • Hartmann M, Kim D, Bernsdorff F, Ajami-Rashidi Z, Scholten N, Schreiber S, Zeier T, Schuck S, Reichel-Deland V, Zeier J (2017) Biochemical principles and functional aspects of pipecolic acid biosynthesis in plant immunity. Plant Physiol 174:124–153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann M, Zeier J (2018) l-lysine metabolism to N-hydroxypipecolic acid: an integral immune-activating pathway in plants. Plant J 96:5–21

    CAS  PubMed  Google Scholar 

  • Hartmann M, Zeier T, Bernsdorff F, Reichel-Deland V, Kim D, Hohmann M, Scholten N, Schuck S, Bräutigam A, Hölzel T (2018) Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173(456–469):e16

    Google Scholar 

  • Hilfiker O, Groux R, Bruessow F, Kiefer K, Zeier J, Reymond P (2014) Insect eggs induce a systemic acquired resistance in Arabidopsis. Plant J 80:1085–1094. https://doi.org/10.1111/tpj.12707

    Article  CAS  PubMed  Google Scholar 

  • Howe R, Currie J (1964) Some laboratory observations on the rates of development, mortality and oviposition of several species of Bruchidae breeding in stored pulses. Bull Entomol Res 55:437–477

    Google Scholar 

  • Isaacs M, Carella P, Faubert J, Champigny MJ, Rose JK, Cameron RK (2016) Orthology analysis and in vivo complementation studies to elucidate the role of DIR1 during systemic acquired resistance in Arabidopsis thaliana and Cucumis sativus. Frontiers in plant science 7:566

    PubMed  PubMed Central  Google Scholar 

  • Izaddoost M, Harris BG, Gracy R (1976) Structure and toxicity of alkaloids and amino acids of Sophora secundiflora. J Pharm Sci 65:352–354

    CAS  PubMed  Google Scholar 

  • Jiménez JC, de la Fuente M, Ordás B, Domínguez LEG, Malvar RA (2017) Resistance categories to Acanthoscelides obtectus (Coleoptera: Bruchidae) in tepary bean (Phaseolus acutifolius), new sources of resistance for dry bean (Phaseolus vulgaris) breeding. Crop Protect 98:255–266

    Google Scholar 

  • Kachroo P, Kachroo A (2018) Plants pack a quiver full of arrows. Cell Host Microbe 23:573–575

    CAS  PubMed  Google Scholar 

  • Kamfwa K, Beaver JS, Cichy KA, Kelly JD (2018) QTL mapping of resistance to bean weevil in common bean. Crop Sci 58:1–9

    CAS  Google Scholar 

  • Keneni G, Bekele E, Getu E, Imtiaz M, Damte T, Mulatu B, Dagne K (2011) Breeding food legumes for resistance to storage insect pests: potential and limitations. Sustainability 3:1399–1415. https://doi.org/10.3390/su3091399

    Article  Google Scholar 

  • Klessig DF, Choi HW, Dempsey DMA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Mol Plant Microbe Interact 31:871–888

    CAS  PubMed  Google Scholar 

  • Kornegay J, Cardona C (1991a) Inheritance of resistance to Acanthoscelides obtectus in a wild common bean accession crossed to commercial bean cultivars. Euphytica 52:103–111. https://doi.org/10.1007/BF00021322

    Article  Google Scholar 

  • Kusolwa P, Myers J (2005) Interspecific hybridization between P. vulgaris and P. acutifolius to transfer bruchid resistance. Annual report.

  • Kusolwa P, Myers J (2011) Seed storage proteins ARL2 and its variants from the apalocus of wild tepary bean G40199 confers resistance to acanthoscellides obtectus when expressed in common beans. Afr Crop Sci J 19:255–265

    Google Scholar 

  • Kusolwa PM, Myers JR (2006) Arcelin-like and-amylase-like inhibitor DNA sequences cosegregate with a novel seed storage protein in Phaseolus vulgaris × P. acutifolius hybrids. Ann Rep-Bean Improv Cooper 49:75

    Google Scholar 

  • Kusolwa PM, Myers JR, Porch TG, Trukhina Y, González-Vélez A, Beaver JS (2016) Registration of AO-1012-29-3-3A red kidney bean germplasm line with bean weevil, BCMV, and BCMNV resistance. J Plant Registr 10:149–153

    Google Scholar 

  • Li C-J, Brownson DM, Mabry TJ, Perera C, Bell EA (1996) Nonprotein amino acids from seeds of Cycas circinalis and Phaseolus vulgaris. Phytochemistry 42:443–445

    CAS  PubMed  Google Scholar 

  • Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CM, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822

    CAS  PubMed  Google Scholar 

  • Mbogo K, Davis J, Myers J (2009) Transfer of the arcelin-phytohaemagglutinin-α amylase inhibitor seed protein locus from tepary bean (Phaseolus acutifolius A. Gray) to common bean (P. vulgaris L.). Biotechnology 8:285–295

    CAS  Google Scholar 

  • Meyer JM, Grobbelaar N (1986) Biosynthesis of pipecolic acid and 4-hydroxypipecolic acid. Phytochemistry 25:1469–1470

    CAS  Google Scholar 

  • Návarová H, Bernsdorff F, Döring A-C, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141. https://doi.org/10.1105/tpc.112.103564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parsons DM, Credland PF (2003) Determinants of oviposition in Acanthoscelides obtectus: a nonconformist bruchid. Physiol Entomol 28:221–231

    Google Scholar 

  • Rekhter D, Mohnike L, Feussner K, Zienkiewicz K, Zhang Y, Feussner I (2019) Enhanced disease susceptibility 5 (EDS5) is required for N-hydroxy pipecolic acid formation. bioRxiv: 630723

  • Romeo JT (1984) Insecticidal imino acids in leaves of Calliandra. Biochem Syst Ecol 12:293–297. https://doi.org/10.1016/0305-1978(84)90052-8

    Article  CAS  Google Scholar 

  • Romeo JT (1998) Functional multiplicity among nonprotein amino acids in Mimosoid legumes: a case against redundancy. Ecoscience 5:287–294

    Google Scholar 

  • Rosenthal G (2012) Plant nonprotein amino and imino acids: biological, biochemical, and toxicological properties. Elsevier, Amsterdam

    Google Scholar 

  • SAS Institute (2017) Version 9.4. SAS Institute, Cary, NC (2017)

  • Schoonhoven AV, Cardona C, Valor J (1983) Resistance to the bean weevil and the Mexican bean weevil (Coleoptera: Bruchidae) in noncultivated common bean accessions. J Econ Entomol 76:1255–1259

    Google Scholar 

  • Servillo L, Giovane A, Balestrieri ML, Ferrari G, Cautela D, Castaldo D (2011) Occurrence of pipecolic acid and pipecolic acid betaine (homostachydrine) in Citrus genus plants. J Agric Food Chem 60:315–321

    PubMed  Google Scholar 

  • Shah J, Chaturvedi R, Chowdhury Z, Venables B, Petros RA (2014) Signaling by small metabolites in systemic acquired resistance. Plant J 79:645–658. https://doi.org/10.1111/tpj.12464

    Article  CAS  PubMed  Google Scholar 

  • Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance.

  • Shan L, He P (2018) Pipped at the post: pipecolic acid derivative identified as SAR regulator. Cell 173:286–287

    CAS  PubMed  Google Scholar 

  • Shea CS, Romeo JT (1991) Nutritional indices: do they explain toxicity of Calliandra amino acids? Florida Entomologist 10–17

  • Singh SP (1981) A key for identification of different growth habits of Phaseolus vulgaris L.

  • Singh V, Roy S, Singh D, Nandi AK (2014) Arabidopsis flowering locus D influences systemic-acquired-resistance-induced expression and histone modifications of WRKY genes. J Biosci 39:119–126

    CAS  PubMed  Google Scholar 

  • Sun T, Busta L, Zhang Q, Ding P, Jetter R, Zhang Y (2018) TGACG-BINDING FACTOR 1 (TGA 1) and TGA 4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD 1) and CALMODULIN-BINDING PROTEIN 60g (CBP 60g). New Phytol 217:344–354

    CAS  PubMed  Google Scholar 

  • Tortosa M, Cartea ME, Rodríguez VM, Velasco P (2018) Unraveling the metabolic response of Brassica oleracea exposed to Xanthomonas campestris pv. campestris. J Sci Food Agric 98:3675–3683

    CAS  PubMed  Google Scholar 

  • Vogel-Adghough D, Stahl E, Návarová H, Zeier J (2013) Pipecolic acid enhances resistance to bacterial infection and primes salicylic acid and nicotine accumulation in tobacco. Plant Signal Behav 8:e26366

    PubMed  PubMed Central  Google Scholar 

  • Wang C, Liu R, Lim G-H, de Lorenzo L, Yu K, Zhang K, Hunt AG, Kachroo A, Kachroo P (2018a) Pipecolic acid confers systemic immunity by regulating free radicals. Sci Adv 4:e4509

    Google Scholar 

  • Wang S, Han K, Peng J, Zhao J, Jiang L, Lu Y, Zheng H, Lin L, Chen J, Yan F (2019) NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana. Mol Plant Pathol.

  • Wang Y, Schuck S, Wu J, Yang P, Döring A-C, Zeier J, Tsuda K (2018b) A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30:2480–2494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Ludewig U (2014) Lysine catabolism, amino acid transport, and systemic acquired resistance: what is the link? Plant Signal Behav 9:e28933. https://doi.org/10.4161/psb.28933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaugg I, Magni C, Panzeri D, Daminati MG, Bollini R, Benrey B, Bacher S, Sparvoli F (2013) QUES, a new Phaseolus vulgaris genotype resistant to common bean weevils, contains the Arcelin-8 allele coding for new lectin-related variants. Theor Appl Genet 126:647–661

    CAS  PubMed  Google Scholar 

  • Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36:2085–2103

    CAS  PubMed  Google Scholar 

  • Zhu F, Xi D-H, Yuan S, Xu F, Zhang D-W, Lin H-H (2014) Salicylic acid and jasmonic acid are essential for systemic resistance against tobacco mosaic virus in Nicotiana benthamiana. Mol Plant Microbe Interact 27:567–577

    CAS  PubMed  Google Scholar 

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Acknowledgments

José Cruz Jimenez G. is grateful to the National Institute of Forestry, Agriculture and Livestock Research (INIFAP) and the National Council for Science and Technology (CONACYT) in Mexico for the fellowship that supported his Ph.D. research.

Funding

This research was funded by the Plan Estatal de Ciencia y Tecnología de España within the projects AGL2015-67313-C2-1-R and AGL2016-77628-R funded in part by the European Regional Development Fund.

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Authors and Affiliations

  1. Misión Biológica de Galicia, Spanish National Research Council (CSIC), 36080 Apartado 28, Pontevedra, Spain

    José Cruz Jiménez-Galindo, María Tortosa, Pablo Velasco, María De La Fuente, Bernardo Ordás & Rosa Ana Malvar

  2. Sitio Experimental Sierra de Chihuahua, National Institute of Forestry Agriculture and Livestock Research (INIFAP), Ave. Hidalgo 1213, Cd. Cuauhtémoc, 31500, Chihuahua, Mexico

    José Cruz Jiménez-Galindo

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  1. José Cruz Jiménez-Galindo
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  2. María Tortosa
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  3. Pablo Velasco
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  4. María De La Fuente
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  5. Bernardo Ordás
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  6. Rosa Ana Malvar
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Contributions

JCJG and RAM conceived the study and discussed the results. JCJG carried out field experiments and performed statistical analysis of the data. JCJG drafted the initial manuscript. MT and PV designed and analysed the bioassays for metabolomics analyses. RAM, BO, MF, MT and PV edited the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to José Cruz Jiménez-Galindo.

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Jiménez-Galindo, J.C., Tortosa, M., Velasco, P. et al. Inheritance and metabolomics of the resistance of two F2 populations of Phaseolus spp. to Acanthoscelides obtectus. Arthropod-Plant Interactions 14, 641–651 (2020). https://doi.org/10.1007/s11829-020-09776-3

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