Impact of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) infestation and wounding on gene expression of defense-related genes and chlorophyll fluorescence in common bean
Abdurrahman Sami Koca
A * , Vahdettin Çiftçi B and Mehmet Zahit Yeken B
A
B
Abstract
Plants have evolved complex defense mechanisms against biotic stressors. Many plant defense-related genes that play crucial roles in regulating defense responses have been identified in common bean (Phaseolus vulgaris L.). However, the functional roles of phenylalanine ammonia-lyase (PvPAL), lipoxygenase (PvLOX), glutathione S-transferase (PvGST) and peroxidase (PvPOD) in response to herbivory and wounding remain unclear in common bean. In this study, we investigated the expression patterns of PvPAL, PvLOX, PvGST and PvPOD genes in common bean under wounding and infestation by a major pest, Helicoverpa armigera, using quantitative real-time PCR (qRT-PCR) for the first time. The expression patterns of these genes in response to insect attack and wounding were compared. Moreover, the effects of wounding and H. armigera on the chlorophyll fluorescence parameters (Fv/Fm, PIABS, ABS/RC, TRo/RC, ETo/RC and DIo/RC) were also determined in common bean. Our results revealed that all genes were significantly upregulated in response to H. armigera, whereas PvPAL and PvPOD were downregulated in wounding. Notably, PvLOX and PvGST genes may play significant roles in the defense system of common bean against both wounding and H. armigera infestation. Furthermore, significant reductions in Fv/Fm, PIABS and ETo/RC were determined under both wounding and H. armigera infestation. These findings suggest that H. armigera is more severe than wounding, leading to distinct gene expression profiles and photosynthetic responses in common bean. The study provides valuable insights for both researchers and breeders in future studies associated with insect stress and resilience breeding efforts.
Keywords: biotic stress, common bean, defensive response, gene expression, Helicoverpa armigera, herbivory attack, insect-plant interaction, photosynthetic response.
References
Arnemann JA, James WJ, Walsh TK, Guedes JVC, Smagghe G, Castiglioni E, Tay WT (2016) Mitochondrial DNA COI characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) from Paraguay and Uruguay. Genetics and Molecular Research 15(2), 1-8.
| Crossref | Google Scholar |
Arnemann JA, Roxburgh S, Walsh T, Guedes J, Gordon K, Smagghe G, Tay WT (2019) Multiple incursion pathways for Helicoverpa armigera in Brazil show its genetic diversity spreading in a connected world. Scientific Reports 9(1), 19380.
| Crossref | Google Scholar | PubMed |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89-113.
| Crossref | Google Scholar | PubMed |
Borges A, Melotto M, Tsai SM, Caldas DGG (2012a) Changes in spatial and temporal gene expression during incompatible interaction between common bean and anthracnose pathogen. Journal of Plant Physiology 169(12), 1216-1220.
| Crossref | Google Scholar |
Borges A, Tsai SM, Caldas DGG (2012b) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Reports 31, 827-838.
| Crossref | Google Scholar |
Bussotti F, Strasser RJ, Schaub M (2007) Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. Environmental Pollution 147(3), 430-437.
| Crossref | Google Scholar | PubMed |
Christen D, Schönmann S, Jermini M, Strasser RJ, Défago G (2007) Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. Environmental and Experimental Botany 60(3), 504-514.
| Crossref | Google Scholar |
Dai Y, Shao M, Hannaway D, Wang L, Liang J, Hu L, Lu H (2009) Effect of Thrips tabaci on anatomical features, photosynthetic characteristics and chlorophyll fluorescence of Hypericum sampsonii leaves. Crop Protection 28, 327-332.
| Crossref | Google Scholar |
Dalal PK, Arora R (2021) Fecundity and life-table parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on tomato crop under alternating temperature regimes: implications for pest monitoring in sub-tropical India. International Journal of Tropical Insect Science 41, 2851-2865.
| Crossref | Google Scholar |
Feng H, Wu X, Wu B, Wu K (2009) Seasonal migration of Helicoverpa armigera (Lepidoptera: Noctuidae) over the Bohai Sea. Journal of Economic Entomology 102(1), 95-104.
| Crossref | Google Scholar | PubMed |
Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytologist 167(2), 353-376.
| Crossref | Google Scholar | PubMed |
Golan K, Rubinowska K, Kmieć K, Kot I, Górska-Drabik E, Łagowska B, Michałek W (2015) Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species. Arthropod-Plant Interactions 9, 55-65.
| Crossref | Google Scholar |
Gonçalves JFC, Santos UM, Jr, Nina AR, Jr, Chevreuil LR (2007) Energetic flux and performance index in copaiba (Copaifera multijuga Hayne) and mahogany (Swietenia macrophylla King) seedlings grown under two irradiance environments. Brazilian Journal of Plant Physiology 19(3), 171-184.
| Crossref | Google Scholar |
Grebner W, Stingl NE, Oenel A, Mueller MJ, Berger S (2013) Lipoxygenase6-dependent oxylipin synthesis in roots is required for abiotic and biotic stress resistance of Arabidopsis. Plant Physiology 161(4), 2159-2170.
| Crossref | Google Scholar | PubMed |
Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, Mornhinweg DW (2009) Physiological responses of resistant and susceptible barley, Hordeum vulgare to the Russian wheat aphid, Diurpahis noxia (Mordvilko). Arthropod-Plant Interactions 3, 233-240.
| Crossref | Google Scholar |
Hu F, Zhang Y, Guo J (2023) Identification and characterization of lipoxygenase (LOX) genes involved in abiotic stresses in yellow horn. PLoS ONE 18(10), e0292898.
| Crossref | Google Scholar |
Hussain S, Iqbal N, Pang T, Khan MN, Liu W-G, Yang W-Y (2019a) Weak stem under shade reveals the lignin reduction behavior. Journal of Integrative Agriculture 18(3), 496-505.
| Crossref | Google Scholar |
Hussain S, Iqbal N, Brestic M, Raza MA, Pang T, Langham DR, Safdar ME, Ahmed S, Wen B, Gao Y, Liu W, Yang W (2019b) Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. Science of the Total Environment 658, 626-637.
| Crossref | Google Scholar |
Hussain S, Shuxian L, Mumtaz M, Shafiq I, Iqbal N, Brestic M, Shoaib M, Sisi Q, Li W, Mei X, Bing C, Zivcak M, Rastogi A, Skalicky M, Hejnak V, Weiguo L, Wenyu Y (2021) Foliar application of silicon improves stem strength under low light stress by regulating lignin biosynthesis genes in soybean (Glycine max (L.) Merr.). Journal of Hazardous Materials 401, 123256.
| Crossref | Google Scholar |
Jin T, Sun Y, Zhao R, Shan Z, Gai J, Li Y (2019) Overexpression of peroxidase gene GsPRX9 confers salt tolerance in soybean. International Journal of Molecular Sciences 20(15), 3745.
| Crossref | Google Scholar | PubMed |
Jones CM, Papanicolaou A, Mironidis GK, Vontas J, Yang Y, Lim KS, Oakeshott JG, Bass C, Chapman JW (2015) Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest. Molecular Ecology 24(19), 4901-4911.
| Crossref | Google Scholar | PubMed |
Kerchev PI, Fenton B, Foyer CH, Hancock RD (2011) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant, Cell & Environment 35(2), 441-453.
| Crossref | Google Scholar |
Koca AS (2024) Efficacy of native entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) against Helicoverpa armigera (Hübner, 1808) (Lepidoptera: Noctuidae). Turkish Journal of Entomology 48(4), 451-475.
| Crossref | Google Scholar |
Korth KL, Dixon RA (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiology 115(4), 1299-1305.
| Crossref | Google Scholar | PubMed |
Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Frontiers in Plant Science 9, 751.
| Crossref | Google Scholar | PubMed |
Li Q, Tan W, Xue M, Zhao H, Wang C (2013) Dynamic changes in photosynthesis and chlorophyll fluorescence in Nicotiana tabacum infested by Bemisia tabaci (Middle East–Asia Minor 1) nymphs. Arthropod-Plant Interactions 7, 431-443.
| Crossref | Google Scholar |
Li Q, Sun X, Tan W, Liang Y, Cao H, Wang D (2024) RuBisCO activase alleviates adverse effects of Nilaparvata lugens feeding on photosynthesis in Oryza sativa. Arthropod-Plant Interactions 18, 211-226.
| Crossref | Google Scholar |
Lim CW, Han S-W, Hwang IS, Kim DS, Hwang BK, Lee SC (2015) The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant & Cell Physiology 56(5), 930-942.
| Crossref | Google Scholar | PubMed |
Liu Y, Shi A, Chen Y, Xu Z, Liu Y, Yao Y, Wang Y, Jia B (2025) Beneficial microorganisms: regulating growth and defense for plant welfare. Plant Biotechnology Journal 23(3), 986-998.
| Crossref | Google Scholar | PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4), 402-408.
| Crossref | Google Scholar | PubMed |
Maher EA, Bate NJ, Ni W, Elkind Y, Dixon RA, Lamb CJ (1994) Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proceedings of the National Academy of Sciences 91(16), 7802-7806.
| Crossref | Google Scholar |
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51(345), 659-668.
| Crossref | Google Scholar | PubMed |
Mayo S, Gutierrez S, Malmierca MG, Lorenzana A, Campelo MP, Hermosa R, Casquero PA (2015) Influence of Rhizoctonia solani and Trichoderma spp. in growth of bean (Phaseolus vulgaris L.) and in the induction of plant defense-related genes. Frontiers in Plant Science 6, 685.
| Crossref | Google Scholar | PubMed |
Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Issakidis-Bourguet E, Renou J-P, Noctor G (2010) Arabidopsis Glutathione Reductase1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiology 153(3), 1144-1160.
| Crossref | Google Scholar | PubMed |
Mika A, Boenisch MJ, Hopff D, Lüthje S (2010) Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors. Journal of Experimental Botany 61(3), 831-841.
| Crossref | Google Scholar | PubMed |
Mou Y, Sun Q, Yuan C, Zhao X, Wang J, Yan C, Li C, Shan S (2022) Identification of the LOX gene family in peanut and functional characterization of AhLOX29 in drought tolerance. Frontiers in Plant Science 13, 832785.
| Crossref | Google Scholar | PubMed |
Murúa MG, Scalora FS, Navarro FR, Cazado LE, Casmuz A, Villagrán ME, Lobos E, Gastaminza G (2014) First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomologist 97(2), 854-856.
| Crossref | Google Scholar |
Murúa MG, Fogliata SV, Herrero MI, Vera MA, Casmuz AS, Sosa-Gomez DR (2021) Biological and reproductive parameters of Helicoverpa armigera and Helicoverpa zea reared on artificial diet in Argentina. Bulletin of Insectology 74(1), 55-64.
| Google Scholar |
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. Journal of Integrative Plant Biology 52(2), 195-204.
| Crossref | Google Scholar | PubMed |
Oliveira MB, De Andrade RV, Grossi-de-Sá MF, Petrofeza S (2015) Analysis of genes that are differentially expressed during the Sclerotinia sclerotiorum Phaseolus vulgaris interaction. Frontiers in Microbiology 6, 1162.
| Crossref | Google Scholar | PubMed |
Peng C, Xu W, Wang X, Meng F, Zhao Y, Wang Q, Wang X, Lodi RS, Dong X, Zhu C, Peng L (2025) Alginate oligosaccharides trigger multiple defense responses in tobacco and induce resistance to Phytophthora infestans. Frontiers in Plant Science 16, 1506873.
| Crossref | Google Scholar | PubMed |
Rasmann S, Agrawal AA (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Current Opinion in Plant Biology 12(4), 473-478.
| Crossref | Google Scholar | PubMed |
Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. The Plant Cell 12(5), 707-719.
| Crossref | Google Scholar | PubMed |
Riaz S, Johnson JB, Ahmad M, Fitt GP, Naiker M (2021) A review on biological interactions and management of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Applied Entomology 145(6), 467-498.
| Crossref | Google Scholar |
Sharma HC, Sujana G, Manohar Rao D (2009) Morphological and chemical components of resistance to pod borer, Helicoverpa armigera in wild relatives of pigeonpea. Arthropod-Plant Interactions 3, 151-161.
| Crossref | Google Scholar |
Singh A, Singh IK, Verma PK (2008) Differential transcript accumulation in Cicer arietinum L. in response to a chewing insect Helicoverpa armigera and defence regulators correlate with reduced insect performance. Journal of Experimental Botany 59(9), 2379-2392.
| Crossref | Google Scholar | PubMed |
Singh IK, Kumar S, Singh S, Singh A (2017) Expression profiling of mitogen-activated protein kinase genes from chickpea (Cicer arietinum L.) in response to Helicoverpa armigera, wounding and signaling compounds. Journal of Asia-Pacific Entomology 20(3), 942-948.
| Crossref | Google Scholar |
Specht A, Sosa-Gomez DR, Rios DAM, Claudino VCM, Paula-Moraes SV, Malaquias JV, Silva FAM, Roque-Specht VF (2021) Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil: the big outbreak monitored by light traps. Neotropical Entomology 50, 53-67.
| Crossref | Google Scholar | PubMed |
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16(1), 53-60.
| Crossref | Google Scholar | PubMed |
Tang JY, Zielinski RE, Zangerl AR, Crofts AR, Berenbaum MR, DeLucia EH (2006) The differential effects of herbivory by first and fourth instars of Trichoplusia ni (Lepidoptera: Noctuidae) on photosynthesis in Arabidopsis thaliana. Journal of Experimental Botany 57(3), 527-536.
| Crossref | Google Scholar | PubMed |
Urban L, Aarrouf J, Bidel LPR (2017) Assessing the effects of water deficit on photosynthesis using parameters derived from measurements of leaf gas exchange and of chlorophyll a fluorescence. Frontiers in Plant Science 8, 2068.
| Crossref | Google Scholar | PubMed |
Usha Rani P, Jyothsna Y (2010) Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiologiae Plantarum 32, 695-701.
| Crossref | Google Scholar |
Valencia WM, Pandit A (2024) Photosystem II subunit S (PsbS): a nano regulator of plant photosynthesis. Journal of Molecular Biology 436(5), 168407.
| Crossref | Google Scholar |
Verpoorte R (2000) Secondary metabolism. In ‘Metabolic engineering of plant secondary metabolism’. (Eds R Verpoorte, AW Alfermann) pp. 1–29. (Springer Netherlands: Dordrecht). 10.1007/978-94-015-9423-3_1
Wally O, Punja ZK (2010) Enhanced disease resistance in transgenic carrot (Daucus carota L.) plants over-expressing a rice cationic peroxidase. Planta 232, 1229-1239.
| Crossref | Google Scholar | PubMed |
Wang F, Xu H, Zhang L, Shi Y, Song Y, Wang X, Cai Q, He W, Xie H, Zhang J (2023) The lipoxygenase OsLOX10 affects seed longevity and resistance to saline-alkaline stress during rice seedlings. Plant Molecular Biology 111, 415-428.
| Crossref | Google Scholar | PubMed |
War AR, Paulraj MG, War MY, Ignacimuthu S (2012) Differential defensive response of groundnut germplasms to Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Journal of Plant Interactions 7, 45-55.
| Crossref | Google Scholar |
Wei L, Jin X, Chen XY (2003) Advances in the research of physiological significances and genetic regulation of lignin metabolism. Acta Botanica Boreali-Occidentalia Sinica 23, 675-681.
| Google Scholar |
Wu Y, Yang Z, How J, Xu H, Chen L, Li K (2017) Overexpression of a peroxidase gene (AtPrx64) of Arabidopsis thaliana in tobacco improves plant’s tolerance to aluminum stress. Plant Molecular Biology 95, 157-168.
| Crossref | Google Scholar | PubMed |
Xing Q, Liao J, Cao S, Li M, Lv T, Qi H (2020) CmLOX10 positively regulates drought tolerance through jasmonic acid -mediated stomatal closure in oriental melon (Cucumis melo var. makuwa Makino). Scientific Reports 10, 17452.
| Crossref | Google Scholar | PubMed |
Yeken MZ, Çelik A, Emiralioğlu O, Çiftçi V, Baloch FS, Özer G (2024) Exploring differentially expressed genes in Phaseolus vulgaris L. during BCMV infection. Physiological and Molecular Plant Pathology 130, 102238.
| Crossref | Google Scholar |
Zalucki MP, Murray DAH, Gregg PC, Fitt GP, Twine PH, Jones C (1994) Ecology of Helicoverpa-armigera (Hubner) and Heliothis-punctigera (Wallengren) in the inland of Australia – larval sampling and host-plant relationships during winter and spring. Australian Journal of Zoology 42(3), 329-346.
| Crossref | Google Scholar |
Zhang S-Z, Hua B-Z, Zhang F (2008) Induction of the activities of antioxidative enzymes and the levels of malondialdehyde in cucumber seedlings as a consequence of Bemisia tabaci (Hemiptera: Aleyrodidae) infestation. Arthropod-Plant Interactions 2, 209-213.
| Crossref | Google Scholar |
Zhao X, She X, Du Y, Liang X (2007) Induction of antiviral resistance and stimulary effect by oligochitosan in tobacco. Pesticide Biochemistry and Physiology 87(1), 78-84.
| Crossref | Google Scholar |
Zhou J, Zhou J, Jr, Wu B, Qin P, Qi A (2010) Physiological factors for tolerance of Kosteletzkya virginica (L.) Presl to one-instar bollworms of Helicoverpa armigera (Hubner). Acta Physiologiae Plantarum 32, 519-529.
| Crossref | Google Scholar |
