Abstract
To investigate physiological and biochemical changes of thrips-resistant alfalfa (Medicago sativa L. cv. Gan-nong No. 9), we aimed at clarifying the response mechanisms of alfalfa against thrips. Medicago sativa L. cv. including thrips-resistant Gan-nong No.9 (G9), thrips-susceptible Gan-nong No.3 (G3) and highly thrips-susceptible WL363HQ (363) were infested with different thrips densities (3, 5, 7 and 9-thrips per branch). The quantitative change in specific nutrients, secondary metabolites, defensive and antioxidant enzymes were measured at seedling stage of the three alfalfa cultivars. The results showed that with the increase of thrips densities, the damage indices, SS, Pro, flavonoids, tannin and H2O2 in G9, G3 and 363 were significantly increased, but PPO and SOD significantly reduced, compared with CK. Furthermore, the tannin and lignin contents of G9 were significantly higher compared to 363, but SP content was significantly lower than G3 and H2O2 content which was further significantly less compared to 363. Correlation analysis observed that the damage index of the three alfalfa cultivars showed a significant positive association with SS, Pro, flavone, tannin, and H2O2 (P < 0.01), while damage index and DW, Chl (a, b, a + b), PPO and SOD showed a significant negative correlation (P < 0.01). Based on principal component comprehensive evaluation, the 5-thrips adults per branch were the critical inoculation threshold for G9 against thrips injury because the score was – 0.048. These results revealed that thrips damage significantly increased the contents of SS, Pro, flavonoids, tannins and H2O2, as well as significantly declined the activities of PPO and SOD in the three cultivars (P < 0.05), moreover, thrips-resistant G9 markedly accumulated lignin content, POD and CAT activity, inhibited Chl (a + b, b) and SP biosynthesis to resist thrips damage.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aljbory Z, Chen MS (2017) Indirect plant defense against insect herbivores: a review. Insect Sci. https://doi.org/10.1111/1744-7917.12436
Bai Y, Gao XK, Wang YC, Chen ZC, Sun J, Wan FH, Yuan ZL (2015) Field comparison of the resistance of 33 alfalfa cultivars to thrips. Acta Prataculturae Sin 24(3):187–194
Bailly C, Benamar A, Corbineau F, Come D (2006) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97(1):104–110. https://doi.org/10.1111/j.1399-3054.1996.tb00485.x
Barros JRA, Guimares MJM, Silva RME, Melo NFD, Rego MTC, Angelotti F (2021) Selection of cowpea cultivars for high temperature tolerance: physiological, biochemical and yield aspects. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-020-00919-7
Bates LS, Waldren SP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bruce RJ, West CA (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol 91(3):889–897. https://doi.org/10.1104/pp.91.3.889
Carcamo HA, Vankosky MA, Asha W, Olfert OO, Meers SB, Evenden ML (2018) Progress toward integrated pest management of pea leaf weevil: a review. Ann Entomol Soc Am 111:144–153. https://doi.org/10.1093/aesa/say007
Cheng KC, Wu JY, Lin JT, Liu WH (2013) Enhancements of isoflavone aglycones, total phenolic content, and antioxidant activity of black soybean by solid-state fermentation with Rhizopus spp. Eur Food Res Technol 236(6):1107–1113. https://doi.org/10.1007/s00217-013-1936-7
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431. https://doi.org/10.1016/0076-6879(90)86135-I
FAO (UN Food and Agriculture Organization) (2009) Global agriculture towards 2050. High Level Expert Forum FAO, Rome
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. https://doi.org/10.1051/agro:2008021
Furstenberg HJ, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297. https://doi.org/10.3390/ijms140510242
Giannopolitis CN, Ries SK (1977) Superoxide dismutase: I. occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Gulsen O, Eickhoff T, Heng-Moss T, Shearman R, Baxendale F, Sarath G, Lee D (2010) Characterization of peroxidase changes in resistant and susceptible warm-season turfgrasses challenged by Blissus occiduus. Arthropod Plant Interact 4:45–55. https://doi.org/10.1007/s11829-010-9086-3
He CG, Cao ZZ, Wu JF, Wang SS (2005) History, achievement and prospect of alfalfa insect pest research in China. Pratacultural Sci 22(4):75–78
He CG, Wang SS, Cao ZZ, Wei ZW, Feng HW (2007) Field evaluation on resistance of 40 Medicago cultivars(lines) to thrips. Acta Prataculturae Sin 16(5):79–83
He J, Chen F, Chen S, Lv G, Deng F, Fang W, Liu Z, Guan Z, He C (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation[J]. J Plant Physiol 168(7):693. https://doi.org/10.1016/j.jplph.2010.10.009
Hedin PA, Jenkins JN, Parrott WL (1992) Evaluation of flavonoids in Gossypium arboretum (L.) cottons as potential source of resistance to tobacco budworm. J Chem Ecol 18(2):105–114. https://doi.org/10.1007/BF00993746
Heng MT, Sarath G, Baxendale FP, Novak D, Bose S, Ni XH, Quisenberry S (2004) Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus. J Econ Entomol 97(3):1086–1095. https://doi.org/10.1603/0022-0493(2004)097[1086:COOECI]2.0.CO;2
Hu GX, He CG, Wang SS, Du WH (2007) Study on resistance mechanism of Medicago sativa to Odontothrips loti. Pratacultural Sci 24(9):86–89
Jan B, Roel M (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44(267):1627–1629. https://doi.org/10.1093/jxb/44.10.1627
Kou JT (2012) Study of physiological and biochemical response of alfalfa to Odontothrips loti Damage, Gansu Agricultural University master dissertation 6
Li Q, He Y, Yang QF, Jiang CX, Wang HJ, Jiang SR (2015) Relationships between several secondary substances in pepper cultivars and the resistance to broad mite Polyphagotarsonemus latus (Banks). J Plant Prot 42(02):283–288
Li TT, Jiang WZ, Gu TT, Liu YY, Xu JP, Liu GJ, Cao CX (2016) Relationship between aphid-resistance and leaf nutrient content of cucumber. Shandong Agric Sci 48(10):44–47
Liu J (2013) Cloning and expression analysis of phenylalanine ammonialyase gene (PAL) from Cucurbita pepo and the study on cultivars. Gansu Agricultural University Doctor dissertation 6
Liu YL (2009) Resistant mechanism research of anti-thrips new strain of alfalfa. Inner Mongolia Agricultural University Doctor dissertation 6
Lu Y, Wang HQ, Chen LS, Wang PL, Li J (2017) Correlation between induced resistance to aphids and secondary metabolism enzyme activities of cotton cultivars in Xinjiang. Plant Prot 43(3):51–55
Ma ML, Karsani SA, Mohajer S, Malek SNA (2014) Phytochemical constituents, nutritional values, phenolics, flavonols, flavonoids, antioxidant and cytotoxicity studies on Phaleria macrocarpa (Scheff) Boerl fruits. BMC Complement Altern Med 14(8):1187–1198. https://doi.org/10.1186/1472-6882-14-152
Mansour MH, Zohdy MN, EI-Gengaihi S E, Amr A E, (1997) The relationship between tannins concentration in some cotton cultivars and susceptibility to piercing sucking insects. J Appl Entomol 121:321–325. https://doi.org/10.1111/j.1439-0418.1997.tb01413.x
Mauchmani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of arabidopsis to peronospora parasitica. Plant Cell 8(2):203–212. https://doi.org/10.1105/tpc.8.2.203
Mayer AM, Harel E (1979) Polyphenol oxidases in plant. Phytochemistry 18:193–215. https://doi.org/10.1016/0031-9422(79)80057-6
Moctezuma C, Hammerbacher A, Heil M, Gershenzon J, Mendez-Alonzo R, Oyama K (2014) Specific polyphenols and tannins are associated with defense against insect herbivores in the tropical Oak Quercus oleoides. J Chem Ecol 40(5):458–467. https://doi.org/10.1007/s10886-014-0431-3
Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89. https://doi.org/10.1146/annurev.ento.51.110104.151044
Mound LA (2005) Thysanoptera: diversity and interactions. Annu Rev Entomol 50:247–269. https://doi.org/10.1146/annurev.ento.49.061802.123318
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Pang HC (2017) Studies on resistance of pepper cultivars to Frankliniella occidentalis. Ningxia University master dissertation 5
Penella C, Nebauer SG, Bautista AS, Lopez-Galarza S, Calatayud A (2014) Rootstock alleviates PEG-induced water stress in grafted pepper seedlings: physiological responses. J Plant Physiol 171:842–851. https://doi.org/10.1016/j.jplph.2014.01.013
Peng R, Zeng WF, Li YS, Cui XN, Hu GX (2019) Effects of phosphorus application on alfalfa photosynthesis and resistance to thrips (Thysanopterra: Thripidae). Plant Prot 45(6):201–207
Reddy GVP (2018) Special issue on pulse crop insect pests and their management strategies: an emerging concern. Ann Entomol Soc Am 111:137–138. https://doi.org/10.1093/aesa/say016
Rehman F, Khan FA, Badruddin S (2012) Role of phenolics in plant defense against insect herbivory. Chemistry of phytopotentials: health energy and environmental perspectives. Springer, Berlin
Shannon LM, Kay E, Lew JY (1966) Peroxidase isozymes from horse radish roots: I. Isolation and physical properties. J Biol Chem 241:2166–2172. https://doi.org/10.1016/S0021-9258(18)96680-9
Steenbergen M, Abd-El-Haliem A, Bleeker P, Dicke M, Escobar-Bravo R, Cheng G, Haring MA, Kant MR, Kappers I, Klinkhamer PGL (2018) Thrips advisor: exploiting thrips-induced defences to combat pests on crops. J Exp Bot 8:1–12. https://doi.org/10.1093/jxb/ery060
Stuart RR, Gao YL, Lei ZR (2011) Thrips: pests of concern to China and the United States. J Integr Agric 10(6):867–892. https://doi.org/10.1016/S1671-2927(11)60073-4
Todd GW, Getahun A, Cress DC (1971) Resistance in barley to the Greenbug, Schizaphis graminum. 1 toxicity of phenolic and flavonoid compounds and related substances. Ann Entomol Soc Am 64(3):718–722. https://doi.org/10.1093/aesa/64.3.718
Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4(3):147–157. https://doi.org/10.1007/s10311-006-0068-8
Tu XB, Fan YL, Ji MS, Liu ZK, Xie N, Liu ZY, Zhang ZH (2015) Improving a method for evaluating alfalfa cultivar resistance to thrips. J Integr Agric. https://doi.org/10.1016/S2095-3119(15)61197-2
Wang J, Song YY, Hu L, Yang MY, Zeng RS (2018) Plant anti-herbivore defense priming: concept, mechanisms and application. Chin J Appl Ecol 29(6):2068–2078
Wang Q (2008) Effects of Odontothrips loti damage on growth of alfalfa cultivars. Gansu Agricultural University master dissertation 6
Wang XS (2014) Effect of Odontothrips loti feeding on the secondary metabolites content in alfalfa leaf. Gansu Agricultural University master dissertation 6
Wang XS, Yang CL, Wang SS, Hu GX (2014) Changes of phenols and lignin contents in alfalfa leaf damaged by Odontothrips loti. Chin J Appl Ecol 25(06):1688–1692
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7(10):1306–1320. https://doi.org/10.4161/psb.21663
War AR, Paulraj MG, Hussai B, Buhroo AA, Ignacimuthu S, Sharma HC (2013) Effect of plant secondary metabolites on legume pod borer, Helicoverpa armigera. J Pest Sci 86:399–408. https://doi.org/10.1007/s10340-013-0485-y
War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Jasmonic acid-mediated- induced resistance in groundnut (Arachis hypogaea L.) against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). J Plant Growth Regul 30:512–523. https://doi.org/10.1007/s00344-011-9213-0
Wellburn AR, Lichtenthaler HK (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. In: Sybesma C (ed) Advances in photosynthesis research. advances in agricultural biotechnology. Springer, Dordrecht, pp 9–12. https://doi.org/10.1007/978-94-017-6368-4_3
Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Montagu MV, Inze D, Camp WV (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. Eur Mol Biol Org J 16(16):4806–4816. https://doi.org/10.1093/emboj/16.16.4806
Wu DG, Wang SS, Liu CZ, Hu GX, Du JL, He CG (2011) Effects of herbivore stress by Acyrthosiphon pisum on the contents of tannin and physiological activity in different alfalfa cultivars. Acta Agrestia Sin 19(02):351–355
Wu MM, Yang LR, Yang XZ, Zhang X, Ma JX, Zhang Y, Li H (2015) Effect of aphid invasion on physiological and biochemical indexes in watermelon seedling stage. J Fruit Sci 32(5):943–949
Xing GN, Zhao TJ, Gai JY (2008) Inheritance of resistance to Lamprosema indicata (Fabricius) in soybean. Acta Agron Sin 34:8–16
Xu XL (2013) Identification and mechanisms of watermelon resistance to Aphis gossypii glover. Hainan University doctor dissertation 5
Zhang CN, Wu JX, Dai W, Chen L (2005a) Activities of some isoenzymes in the leaves of Brassica oleracea seedlings infested by peach aphid (Myzus persicae). Acta Bot Sin 25:1566–1569
Zhang L, Chang JH, Luo YW (2005b) Activity changes of POD, PPO, PAL of the different sorghum genotypes invaded by aphis sacchari Zehntner. Chin Agric Sci Bull 21(7):40–42
Zhang R, Yang F, Xian CZ, Ma JH, Zhang SH (2005c) A study on the yield loss and economic threshold of alfalfa damaged by thrip Odentothrips Lati. Plant Prot 31(1):47–49
Zhang SZ, Zhang F, Hua BZ (2008) Enhancement of phenylalanine ammonia lyase, polyphenol oxidase, and peroxidase in cucumber seedlings by Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) infestation. Agric Sci China 7(1):82–87. https://doi.org/10.1016/S1671-2927(08)60025-5
Zhang HY, Wei SH, Zhang R, Miao R, Li KC, Luo XL, Zhang Y (2016a) Effects of Acyrthosiphon pisum on enzyme activities and nutrients of different alfalfa cultivars. Pratacultural Sci 33(01):144–152
Zhang XY, Wang SS, Li XL, Li YJ, Hu GX (2016b) Effects of phosphorus application on alfalfa resistance to thrips (Thripidae). Acta Prataculturae Sin 25(5):102–108
Zhu YF, Chen M, Liu CZ (2011) Variations of several substances in the seedlings of five oat cultivars infested by aphids. Plant Protection 37(02):55–58
Acknowledgements
We extremely thanked Professor Shi Shangli of Gansu Agricultural University for his valuable suggestions during the paper writing. This work was supported by Science and Technology Program of Gansu Province (No. 19ZD2NA002), and the Discipline Construction Fund Project of Gansu Agricultural University (No. GAU-XKJS-2018-002).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wu, F., Shi, S., Li, Y. et al. Physiological and biochemical response of different resistant alfalfa cultivars against thrips damage. Physiol Mol Biol Plants 27, 649–663 (2021). https://doi.org/10.1007/s12298-021-00961-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-00961-z