Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-28T18:37:34.567Z Has data issue: false hasContentIssue false

Effects of drought stress and plant cultivar type on demographic characteristics of the rose-grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae)

Published online by Cambridge University Press:  19 October 2022

Maryam Aleosfoor*
Affiliation:
Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, Iran
Maryam Zahediannezhad
Affiliation:
Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, Iran
Kambiz Minaei
Affiliation:
Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, Iran
Lida Fekrat
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
Hooman Razi
Affiliation:
Department of Plant Production and Genetics, School of Agriculture, Shiraz University, Shiraz, Iran
*
Author for correspondence: Maryam Aleosfoor, Email: aosfoor@shirazu.ac.ir

Abstract

Drought is a substantial threat to cereal production under global climatic change scenarios, albeit its aftermath on arthropod pests is yet contentious. To address this issue, demographic characteristics of Metopolophium dirhodum (Walker, 1849) (Hemiptera: Aphididae) were studied on one drought-susceptible wheat cultivar and one drought-tolerant wheat cultivar under different water treatments. Some physiological and biochemical features of wheat cultivars including leaf soluble sugar and proline contents and antioxidant enzymes activities were also investigated. Significant differences occurred in the developmental period, survival, and fecundity of M. dirhodum between wheat cultivars under various water treatments. The impact of intermediate and severe water stress on M. dirhodum was neutral and negative for the tolerant cultivar and negative for the water-susceptible cultivar, respectively. Under severe water stress, on both wheat cultivars, the aphids had low net reproductive rates and finite and intrinsic rates of increase in comparison with those reared on unstressed plants. In total, drought resulted in lower growth of population and reduced survival of aphids. Hence, in the context of projected climatic changes, acute water deficiency could probably result in reducing the abundance and menace of outburst of M. dirhodum. However, it should be noted that the potential likelihood of M. dirhodum eruptions can be drastically affected by the degree of drought intensity and host plant cultivar.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abid, M, Tian, Z, Ata-Ul-Karim, ST, Liu, Y, Cui, Y, Zahoor, R, Jiang, D and Dai, T (2016) Improved tolerance to post-anthesis drought stress by pre-drought priming at vegetative stages in drought-tolerant and -sensitive wheat cultivars. Plant Physiology and Biochemistry 106, 218227.CrossRefGoogle ScholarPubMed
Abid, M, Ali, S, Qi, L-K, Zahoor, R, Tian, Z, Jiang, D, Snider, JL and Dai, T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Scientific Reports 8, 4615.CrossRefGoogle ScholarPubMed
Akköprü, EP, Atlıhan, R, Okut, H and Chi, H (2015) Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology 108, 378387.CrossRefGoogle ScholarPubMed
Atlıhan, R, Kasap, I, Özgökçe, M, Polat Akköprü, E and Chi, H (2017) Population growth of Dysaphis pyri (Hemiptera: Aphididae) on different pear cultivars with discussion on curve fitting in life table studies. Journal of Economic Entomology 110, 18901898.CrossRefGoogle ScholarPubMed
Banfield-Zanin, JA and Leather, SR (2015) Season and drought stress mediate growth and weight of the green spruce aphid on Sitka spruce. Agricultural and Forest Entomology 17, 4856.CrossRefGoogle Scholar
Bates, LS, Waldren, RP and Teare, ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205207.CrossRefGoogle Scholar
Beetge, L and Krüger, K (2019) Drought and heat waves associated with climate change affect performance of the potato aphid Macrosiphum euphorbiae. Scientific Reports 9, 3645.CrossRefGoogle ScholarPubMed
Bowne, JB, Erwin, TA, Juttner, J, Schnurbusch, T, Langridge, P, Bacic, A and Roessner, U (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Molecular Plant 5, 418429.CrossRefGoogle ScholarPubMed
Bussaman, P, Sa-Uth, C, Chandrapatya, A, Atlihan, R, Gökçe, A, Saska, P and Chi, H (2017) Fast population growth in physogastry reproduction of Luciaphorus perniciosus (acari: Pygmephoridae) at different temperatures. Journal of Economic Entomology 110, 13971403.CrossRefGoogle ScholarPubMed
Chi, H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology 17, 2634.CrossRefGoogle Scholar
Chi, H (1990) Timing of control based on the stage structure of pest populations: a simulation approach. Journal of Economic Entomology 83, 11431150.CrossRefGoogle Scholar
Chi, H (2020) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. Retrieved from (140.120.197.173/Ecology/).Google Scholar
Chi, H and Liu, H (1985) Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica 24, 225240.Google Scholar
Chi, H and Su, HY (2006) Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environmental Entomology 35, 1021.CrossRefGoogle Scholar
Chi, H, You, M, Atlıhan, R, Smith, CL, Kavousi, A, Özgökçe, MS, Güncan, A, Tuan, SJ, Fu, JW, Xu, YY, Zheng, FQ, Ye, BH, Chu, D, Yu, Y, Gharekhani, G, Saska, P, Gotoh, T, Schneider, MI, Bussaman, P, Gökçe, A and Liu, TX (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomologia Generalis 40, 103124.CrossRefGoogle Scholar
Chowdhury, MK, Hasan, MA, Bahadur, MM, Islam, MR, Hakim, MA, Iqbal, MA, Javed, T, Raza, A, Shabbir, R, Sorour, S, Elsanafawy, NEM, Anwar, S, Alamri, S, Sabagh, AE and Islam, MS (2021) Evaluation of drought tolerance of some wheat (Triticum aestivum L.) genotypes through phenology, growth, and physiological indices. Agronomy 11, 1792.CrossRefGoogle Scholar
Cohen, I, Zandalinas, S, Huck, C, Fritschi, F and Mittle, RR (2021) Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiologia Plantarum 171, 6676.CrossRefGoogle ScholarPubMed
Cui, H, Wang, L, Reddy, GVP and Zhao, Z (2020) Mild drought facilitates the increase in wheat aphid abundance by changing host metabolism. Annals of the Entomological Society of America 114, 7983.CrossRefGoogle Scholar
Dai, P, Liu, D and Shi, X (2015) Impacts of water deficiency on life history of Sitobion avenae clones from semi-arid and moist areas. Journal of Economic Entomology 108, 22502258.CrossRefGoogle ScholarPubMed
Dale, AG and Frank, SD (2017) Warming and drought combine to increase pest insect fitness on urban trees. PLoS ONE 12, e0173844.CrossRefGoogle ScholarPubMed
Dhindsa, RS, Plumb-Dhindsa, P and Thorpe, TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32, 93101.CrossRefGoogle Scholar
ElSayed, AI, El-Hamahmy, MAM, Rafudeen, MS, Mohamed, AH and Omar, AA (2019) The impact of drought stress on antioxidant responses and accumulation of flavonolignans in milk thistle (Silybum marianum (L.) Gaertn). Plants 8, 611.CrossRefGoogle ScholarPubMed
Giannopolitis, CN and Ries, SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiology 59, 309314.CrossRefGoogle ScholarPubMed
Haile, FJ (2001) Drought stress, insects and yield loss. In Peterson, RKD and Highley, LG (eds), Biotic Stress and Yield Loss. Boca Raton: CRC Press Inc., pp. 117134.Google Scholar
Hale, B, Bale, J, Pritchard, J, Masters, G and Brown, V (2003) Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis. Ecological Entomology 28, 666677.CrossRefGoogle Scholar
Han, P, Lavoir, AV, Rodriguez-Saona, C and Desneux, N (2022) Bottom-up forces in agroecosystems and their potential impact on arthropod pest management. Annual Review of Entomology 67, 239259.CrossRefGoogle ScholarPubMed
Hasanuzzaman, M, Bhuyan Borhannuddin, MHM, Zulfiqar, F, Raza, A, Mohsin, SM, Mahmud, JA, Fujita, M and Fotopoulos, V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9, 681.CrossRefGoogle ScholarPubMed
Hasheminasab, H, Assad, M, Aliakbari, A and Sahhafi, S (2012) Influence of drought stress on oxidative damage and antioxidant defense systems in tolerant and susceptible wheat genotypes. Journal of Agricultural Science 4, 2030.CrossRefGoogle Scholar
Hesterberg, T (2008) It's time to retire the ‘n ≥ 30’ rule. Available at https://static.googleusercontent.com/media/research.google.com/en//pubs/archive/34906.pdf.Google Scholar
Honek, A, Martinkova, Z, Saska, P and Dixon, AFG (2018) Aphids (Homoptera: Aphididae) on winter wheat: predicting maximum abundance of Metopolophium dirhodum. Journal of Economic Entomology 111, 17511759.CrossRefGoogle ScholarPubMed
Howe, GA and Schilmiller, AL (2002) Oxylipin metabolism in response to stress. Current Opinion in Plant Biology 5, 230236.CrossRefGoogle ScholarPubMed
Huang, HW, Chi, H and Smith, CL (2018) Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. Journal of Economic Entomology 111, 19.Google Scholar
Huberty, AF and Denno, RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85, 13831398.CrossRefGoogle Scholar
Kansman, J, Nalam, V, Nachappa, P and Finke, D (2020) Plant water stress intensity mediates aphid host choice and feeding behaviour. Ecological Entomology 45, 14371444.CrossRefGoogle Scholar
Kapoor, D, Bhardwaj, S, Landi, M, Sharma, A, Ramakrishnan, M and Sharma, A (2020) The impact of drought in plant metabolism: how to exploit tolerance mechanisms to increase crop production. Applied Sciences 10, 5692.CrossRefGoogle Scholar
Kuglerová, M, Skuhrovec, J and Münzbergová, Z (2019) Relative importance of drought, soil quality, and plant species in determining the strength of plant-herbivore interactions. Ecological Entomology 44, 665677.CrossRefGoogle Scholar
Lisar, SYS, Motafakkerazad, R, Hossain, MM and Rahman, IMM (2012) Water stress in plants: causes, effects and responses. In Rahman, IMM and Hasegawa, H (eds), Water Stress. London: IntechOpen, pp. 114.Google Scholar
Liu, D, Dai, P, Li, S, Ahmed, SS, Shang, Z and Shi, X (2018) Life-history responses of insects to water-deficit stress: a case study with the aphid Sitobion avenae. BMC Ecology 18, 17.CrossRefGoogle Scholar
Ma, C-S, Hau, B and Poehling, H-M (2004) Effects of pattern and timing of high temperature exposure on reproduction of the rose grain aphid, Metopolophium dirhodum. Entomologia Experimentalis et Applicata 110, 6571.CrossRefGoogle Scholar
Maazou, ARS, Tu, JL, Qiu, J and Liu, ZZ (2016) Breeding for drought tolerance in maize (Zea mays L.). American Journal of Plant Sciences 7, 18581870.CrossRefGoogle Scholar
Maghsoudi, K, Emam, Y and Pessarakli, M (2016) Effect of silicon on photosynthetic gas exchange, photosynthetic pigments, cell membrane stability and relative water content of different wheat cultivars under drought stress conditions. Journal of Plant Nutrition 39, 10011015.CrossRefGoogle Scholar
Malhi, GS, Kaur, M and Kaushik, P (2021) Impact of climate change on agriculture and its mitigation strategies: a review. Sustainability 13, 1318.CrossRefGoogle Scholar
Mao, H, Yang, Y, Guo, C, Zhang, Q and Liu, X (2012) Changes in defensive enzyme expression in cotton leaves activity and defensive enzyme gene after feeding by Apolygus lucorum. Chinese Journal of Applied Entomology 49, 652659.Google Scholar
Marček, T, Hamow, , Végh, B, Janda, T and Darko, E (2019) Metabolic response to drought in six winter wheat genotypes. PLoS ONE 14, e0212411.CrossRefGoogle ScholarPubMed
Maurino, VG and Flügge, UI (2008) Experimental systems to assess the effects of reactive oxygen species in plant tissues. Plant Signaling and Behavior 3, 923928.CrossRefGoogle ScholarPubMed
Mewis, I, Khan, MAM, Glawischnig, E, Schreiner, M and Ulrichs, C (2012) Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PLoS ONE 7, e48661.CrossRefGoogle ScholarPubMed
Moussa, HR and Abdel-Aziz, SM (2008) Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Australian Journal of Crop Science 1, 3136.Google Scholar
Nachappa, P, Culkin, CT, Saya, PM, Han, J and Nalam, VJ (2016) Water stress modulates soybean aphid performance, feeding behavior, and virus transmission in soybean. Frontiers in Plant Science 7, 552.CrossRefGoogle ScholarPubMed
Nakano, Y and Asada, K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867880.Google Scholar
Nowsherwan, I, Shabbir, G, Malik, SI, Ilyas, M, Iqbal, MS and Musa, M (2018) Effect of drought stress on different physiological traits in bread wheat. SAARC Journal of Agriculture 16, 16.CrossRefGoogle Scholar
Osswaldi, WF, Kraus, R, Hippeli, S, Benz, B, Volpert, R and Elstner, EF (1992) Comparison of the enzymatic activities of dehydroascorbic acid reductase, glutathione reductase, catalase, peroxidase and superoxide dismutase of healthy and damaged spruce needles (Picea abies (L.) Karst.). Journal of Plant Physiology 139, 742748.CrossRefGoogle Scholar
Ozden, M, Demirel, U and Kahraman, A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Scientia Horticulturae 119, 163168.CrossRefGoogle Scholar
Özgökçe, MS, Chi, H, Atlıhan, R and Kara, H (2018a) Demography and population projection of Myzus persicae (Sulz.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars. Phytoparasitica 46, 153167.CrossRefGoogle Scholar
Özgökçe, MS, Chi, H, Atlıhan, R and Kara, H (2018b) Correction to: demography and population projection of Myzus persicae (Sulz.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars. Phytoparasitica 46, 169169.CrossRefGoogle Scholar
Payus, C, Ann Huey, L, Adnan, F, Besse Rimba, A, Mohan, G, Kumar Chapagain, S, Roder, G, Gasparatos, A and Fukushi, K (2020) Impact of extreme drought climate on water security in north Borneo: case study of Sabah. Water 12, 1135.CrossRefGoogle Scholar
Pons, C, Voß, AC, Schweiger, R and Müller, C (2020) Effects of drought and mycorrhiza on wheat and aphid infestation. Ecology and Evolution 10, 1048110491.CrossRefGoogle ScholarPubMed
Qayyum, A, Aziz, MA, Iftikhar, A, Hafeez, F and Atlihan, R (2018) Demographic parameters of Lipaphis erysimi (Hemiptera: Aphididae) on different cultivars of brassica vegetables. Journal of Economic Entomology 111, 18851894.CrossRefGoogle ScholarPubMed
Quandahor, P, Lin, C, Gou, Y, Coulter, JA and Liu, C (2019) Leaf morphological and biochemical responses of three potato (Solanum tuberosum l.) cultivars to drought stress and aphid (Myzus persicae sulzer) infestation. Insects 10, 435.CrossRefGoogle ScholarPubMed
Quandahor, P, Gou, Y, Lin, C, Coulter, JA and Liu, C (2021) Comparison of root tolerance to drought and aphid (Myzus persicae Sulzer) resistance among different potato (Solanum tuberosum L.) cultivars. Scientific Reports 11, 628.CrossRefGoogle ScholarPubMed
Raza, A, Mehmood, SS, Shah, T, Zou, X, Yan, L, Zhang, X and Khan, RSA (2019) Applications of molecular markers to develop resistance against abiotic stresses in wheat. In Hasanuzzaman, M, Nahar, K and Hossain, M (eds), Wheat Production in Changing Environments. Singapore: Springer, pp. 393420.CrossRefGoogle Scholar
Rivelli, RA, Trotta, V, Toma, I, Fanti, P and Battaglia, D (2013) Relation between plant water status and Macrosiphum euphorbiae (Hemiptera: Aphididae) population dynamics on three cultivars of tomato. European Journal of Entomology 110, 617625.CrossRefGoogle Scholar
Rouault, G, Candau, JN, Lieutier, F, Nageleisen, LM, Martin, JC and Warzée, N (2006) Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Annals of Forest Science 63, 613624.CrossRefGoogle Scholar
Sallam, A, Alqudah, AM, Dawood, MFA, Baenziger, PS and Börner, A (2019) Drought stress tolerance in wheat and barley: advances in physiology, breeding and genetics research. International Journal of Molecular Sciences 20, 3137.CrossRefGoogle ScholarPubMed
Satishchandra, KN, Chakravarthy, AK, Özgökçe, MS and Atlihan, R (2019) Population growth potential of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomato, potato, and eggplant. Journal of Applied Entomology 143, 518526.CrossRefGoogle Scholar
Sconiers, WB, Rowland, DL and Eubanks, MD (2020) Pulsed drought: the effects of varying water stress on plant physiology and predicting herbivore response. Crop Science 60, 25432561.CrossRefGoogle Scholar
Seleiman, MF, Al-Suhaibani, N, Ali, N, Akmal, M, Alotaibi, M, Refay, Y, Dindaroglu, T, Abdul-Wajid, HH and Battaglia, ML (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10, 259.CrossRefGoogle ScholarPubMed
Shahrokhi Khanghah, S and Amir Moafi, M (2011) Binomial sampling plan of Metopolophium dirhodum in irrigated wheat fields. Applied Entomology and Phytopathology 79, 117133.Google Scholar
Shao, HB, Chu, LY, Abdul Jaleel, C and Zhao, CX (2008) Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus Biologies 331, 215225.CrossRefGoogle ScholarPubMed
Sharma, A, Wang, J, Xu, D, Tao, S, Chong, S, Yan, D, Li, Z, Yuan, H and Zheng, B (2020) Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Science of the Total Environment 713, 136675.CrossRefGoogle ScholarPubMed
Showler, A (2013) Water deficit stress-host plant nutrient accumulations and associations with phytophagous arthropods. In Vahdati, K and Leslie, C (eds), Abiotic Stress – Plant Responses and Applications in Agriculture. IntechOpen: London, pp. 387410.Google Scholar
Showler, A (2014) Plant-arthropod interactions affected by water deficit stress through association with changes. In Gaur, BRK and Sharma, P (eds), Molecular Approaches in Plant Abiotic Stress, 1st Edn. Boca Raton: CRC Press, pp. 339352.Google Scholar
Siahpoosh, MR, Dehghanian, E and Kamgar, A (2011) Drought tolerance evaluation of bread wheat genotypes using water use efficiency, evapotranspiration efficiency, and drought susceptibility index. Crop Science 51, 11981204.CrossRefGoogle Scholar
Simpson, KLS, Jackson, GE and Grace, J (2012) The response of aphids to plant water stress - the case of Myzus persicae and Brassica oleracea var. capitata. Entomologia Experimentalis et Applicata 142, 191202.CrossRefGoogle Scholar
Smucker, MD, Allan, J and Carterette, B (2007) A comparison of statistical significance tests for information retrieval evaluation. Proceedings of the sixteenth ACM conference on information and knowledge management, CIKM, Lisbon, Portugal, pp. 623632.CrossRefGoogle Scholar
Sumner, LC, Need, JT, McNew, RW, Dorschner, KW, Eikenbary, RD and Johnson, RC (1983) Response of Schizaphis graminum (Homoptera: Aphididae) to drought-stressed wheat, using polyethylene glycol as a matricum1. Environmental Entomology 12, 919922.CrossRefGoogle Scholar
Takahashi, F, Kuromori, T, Urano, K, Yamaguchi-Shinozaki, K and Shinozaki, K (2020) Drought stress responses and resistance in plants: from cellular responses to long-distance intercellular communication. Frontiers in Plant Science 11, 556972.CrossRefGoogle ScholarPubMed
Verdugo, JA, Sauge, MH, Lacroze, JP, Francis, F and Ramirez, CC (2015) Drought-stress and plant resistance affect herbivore performance and proteome: the case of the green peach aphid Myzus persicae (Hemiptera: Aphididae). Physiological Entomology 40, 265276.CrossRefGoogle Scholar
Wang, J, Chen, J, Sharma, A, Tao, S, Zheng, B, Landi, M, Yuan, H and Yan, D (2019) Melatonin stimulates activities and expression level of antioxidant enzymes and preserves functionality of photosynthetic apparatus in hickory plants (Carya cathayensis sarg.) under peg-promoted drought. Agronomy 9, 702.CrossRefGoogle Scholar
Wasaya, A, Manzoor, S, Yasir, TA, Sarwar, N, Mubeen, K, Ismail, IA, Raza, A, Rehman, A, Hossain, A and Sabagh A, EL (2021) Evaluation of fourteen bread wheat (Triticum aestivum l.) genotypes by observing gas exchange parameters, relative water and chlorophyll content, and yield attributes under drought stress. Sustainability 13, 4799.CrossRefGoogle Scholar
Watt, AD and Wratten, SD (1984) The effects of growth stage in wheat on yield reductions caused by the rose-grain aphid Metopolophium dirhodum. Annals of Applied Biology 104, 393397.CrossRefGoogle Scholar
Wei, L, Jing, B and Li, H (2020) Bootstrapping promotes the RSFC-behavior associations: an application of individual cognitive traits prediction. Human Brain Mapping 41, 23022316.CrossRefGoogle ScholarPubMed
Wratten, S (1975) The nature of the effects of the aphids Sitobion avenae and Metopolophium dirhodum on the growth of wheat. Annals of Applied Biology 79, 2734.CrossRefGoogle Scholar
Xiaomin, Y, Lijuan, S, Hsin, C, Guodong, K and Changying, Z (2020) Demography of Thrips palmi (Thysanoptera: Thripidae) reared on Brassica oleracea (Brassicales: Brassicaceae) and Phaseolus vulgaris (Fabales: Fabaceae) with discussion on the application of the bootstrap technique in life table research. Journal of Economic Entomology 113, 23902398.Google Scholar
Xie, H, Shi, J, Shi, F, Xu, H, He, K and Wang, Z (2020) Aphid fecundity and defenses in wheat exposed to a combination of heat and drought stress. Journal of Experimental Botany 71, 27132722.CrossRefGoogle ScholarPubMed
Yadav, B, Jogawat, A, Rahman, MS and Narayan, OP (2021) Secondary metabolites in the drought stress tolerance of crop plants: a review. Gene Reports 23, 101040.CrossRefGoogle Scholar
Zhang, Z, Li, H, Zhou, W, Takeuchi, Y and Yoneyama, K (2006) Effect of 5-Aminolevulinic acid on development and salt tolerance of potato (Solanum tuberosum L.) microtubers in vitro. Plant Growth Regulation 49, 2734.Google Scholar
Zhang, Y, Guo, L, Atlıhan, R, Chi, H and Chu, D (2019) Demographic analysis of progeny fitness and timing of resurgence of Laodelphax striatellus after insecticides exposure. Entomologia Generalis 39, 221230.CrossRefGoogle Scholar
Zhang, Y, Wang, LF, Li, TT and Liu, WC (2021) Mutual promotion of LAP2 and CAT2 synergistically regulates plant salt and osmotic stress tolerance. Frontiers in Plant Science 12, 672672.CrossRefGoogle ScholarPubMed
Zhao, H, Sun, X, Xue, M, Zhang, X and Li, Q (2016) Antioxidant enzyme responses induced by whiteflies in tobacco plants in defense against aphids: catalase may play a dominant role. PLoS ONE 11, e0165454.CrossRefGoogle ScholarPubMed
Zhao, W, Liu, L, Shen, Q, Yang, J, Han, X, Tian, F and Wu, J (2020) Effects of water stress on photosynthesis, yield, and water use efficiency in winter wheat. Water 12, 2127.CrossRefGoogle Scholar
Živanović, B, Milić Komić, S, Tosti, T, Vidović, M, Prokić, L and Veljović Jovanović, S (2020) Leaf soluble sugars and free amino acids as important components of abscisic acid-mediated drought response in tomato. Plants 9, 1147.CrossRefGoogle ScholarPubMed