Photosynthetic traits and antioxidative defense responses of Pinus yunnanensis after joint attack by bark beetles Tomicus yunnanensis and T. minor

  • Juan Liu
  • Hang Chen
  • Jianmin Wang
  • Xiaoming Chen
  • Zixiang Yang
  • Junsheng Liang
Original Paper


Bark beetles Tomicus yunnanensis and T. minor are two important pests of Pinus yunnanensis and can cause massive death of pine trees. In this study, we examined several traits related to photosynthesis in P. yunnanensis and their relationship with antibiotic defense responses after joint attack by the two bark beetles at the shoot and the trunk stages. When shoots were attacked by the beetles, the abundance of chlorophylls, carotenoids, and the rates of net photosynthesis (Pn) and transpiration (E) decreased in needles, while the levels of superoxide dismutase and malondialdehyde remained unchanged in both needles and phloem. The activity of peroxidases also remained unchanged in needles, but increased in phloem. The activity of catalases increased in both needles and phloem. When trunks were attacked by the bark beetles, chlorophyll abundance, Pn, E, and antioxidative enzyme activities all declined, and the declines were more pronounced than in the attacked shoots. A decrease in protein concentrations was also observed in needles and phloem from the attacked pines. Attack on shoots by the bark beetles suppressed host defense and provided a favorable environment for larval growth and development, resulting in long-term decline of pine growth potential. The results suggest that attacks on trunks by beetles caused more severe damage to host trees than attacks on shoots.


Antioxidant enzymes Bark beetle Defense responses Photosynthesis Pinus yunnanensis Tomicus minor Tomicus yunnanensis 



We thank Janusz J. Zwiazek and Kirst King-Jones for critical comments on the manuscript.


  1. Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106(30):12311–12316CrossRefGoogle Scholar
  2. Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160(3):283–292CrossRefGoogle Scholar
  3. Chen DL, Zhang X, Jiang BF, Yu PW (2012) Effects on the content of proteins of poplars damaged by Apriona germari (Hope). Biol Disaster Sci 35(1):85–89Google Scholar
  4. David MR, Ursula MRV, Matthew HS, Sharon BG, Carl JB, Donald RO (2014) Biochemical acclimation, stomatal limitation and precipitation patterns underlie decreases in photosynthetic stimulation of soybean (Glycine max) at elevated [CO2] and temperatures under fully open air field conditions. Plant Sci 226:136–146CrossRefGoogle Scholar
  5. Duan Y, Kerdelhue C, Ye H, Lieutier F (2004) Genetic study of the forest pest Tomicus piniperda (Col., Scolytinae) in Yunnan province (China) compared to Europe: new insights for the systematics and evolution of the genus Tomicus. Heredity 93(5):416–422CrossRefGoogle Scholar
  6. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167(2):353–376CrossRefGoogle Scholar
  7. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990(1):87–92CrossRefGoogle Scholar
  8. Gill RS, Gupta AK, Taggar GK, Taggar MS (2010) Role of oxidative enzymes in plant defenses against insect herbivory. Acta Phytopathol Entomol Hung 45(2):277–290CrossRefGoogle Scholar
  9. Glenn EP, Nagler PL, Morino K, Hultine KR (2013) Phreatophytes under stress: transpiration and stomatal conductance of saltcedar (Tamarix, spp.) in a high-salinity environment. Plant Soil 371(1–2):655–672CrossRefGoogle Scholar
  10. Golan K, Rubinowska K, Gorskadrabik E (2013) Physiological and biochemical responses of Fern Nephrolepis Biserrata (Sw.) Schott. To Coccus Hesperidum L. infestation. Acta Biol Crac 55(1):93–98Google Scholar
  11. 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 Interact 9(1):55–65CrossRefGoogle Scholar
  12. Hahlbrock K, Bednarek P, Ciolkowski I, Hamberger B, Heise A, Liedgens H, Logemann E, Nurnberger T, Schmelzer E, Somssich IE, Tan J (2003) Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proc Natl Acad Sci USA 100(2):14569–14576CrossRefGoogle Scholar
  13. Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700CrossRefGoogle Scholar
  14. Hofstetter RW, Mahfouz JB, Klepzig KD, Ayres MP (2005) Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. J Chem Ecol 31(3):539–560CrossRefGoogle Scholar
  15. Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436CrossRefGoogle Scholar
  16. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66CrossRefGoogle Scholar
  17. Huang W, Jia ZK, Han QF (2007) Effects of herbivore stress by Aphis medicaginis Koch on the Malondialdehyde contents and activities of protective enzymes in different alfalfa varieties. Acta Ecol Sin 27(5):2177–2183Google Scholar
  18. Jones HG (1985) Partitioning stomatal and non-stomatal limitations to photosynthesis. Plant Cell Environ 8(2):95–104CrossRefGoogle Scholar
  19. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328CrossRefGoogle Scholar
  20. Kirkendall LR, Faccoli M, Ye H (2008) Description of the Yunnan shoot borer, Tomicus yunnanensis Kirkendall & Faccoli sp. n. (Curculionidae, Scolytinae), an unusually aggressive pine shoot beetle from southern China, with a key to the species of Tomicus. Zootaxa 1819:25–39Google Scholar
  21. Li LS, Wang HL, Chai XS, Wang YX, Shu NB, Yang DS (1993) Study on the biological characteristics of Tomicus yunnanensis and its damage. For Res 6:14–20Google Scholar
  22. Li HS, Sun Q, Zhao SJ (2000) Principles and techniques of plant physiological biochemical experiment, 1st edn. Higher education press, Beijing, pp 134–138Google Scholar
  23. Li LM, Men XY, Ye BH, Yu Y, Zhang AS, Li LL, Zhou XH, Zhuang QY (2014) Defense enxyme activity of Winter Jujube at different stages induced by the damage of Apolygus lucorum. Sci Agric Sin 47(1):191–198Google Scholar
  24. Lieutier F, Yart A, Salle A (2009) Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci 66(8):810CrossRefGoogle Scholar
  25. Liu XP, Ge F, Chen CP, Wang GH, Li ZY (2003) Progress in induced resistance of pines. Sci Silvae Sin 39(5):119–128Google Scholar
  26. Liu YQ, Sun XY, Wang Y, Liu Y (2007) Effects of shades on the photosynthetic characteristics and chlorophyll fluorescence parameters of Urtica dioica. Acts Ecol Sin 27(8):3457–3464Google Scholar
  27. Liu Z, Chen W, He X (2011) Cadmium-induced changes in growth and antioxidative mechanisms of a medicine plant (Lonicera japonica Thunb.). J Med Plants Res 5(8):1411–1417Google Scholar
  28. Lu RC, Wang HB, Zhang Z, Byers JA, Jin YJ, Wen HF, Shi WJ (2012) Coexistence and competition between Tomicus yunnanensis and T. minor (Coleoptera: Scolytinae) in Yunnan pine. Psyche DOI:10:1155/2012/185312Google Scholar
  29. Mitra S, Baldwin IT (2008) Independently silencing two photosynthetic proteins in Nicotiana attenuata has different effects on herbivore resistance. Plant Physiol 148(2):1128–1138CrossRefGoogle Scholar
  30. Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ Exp Bot 53(2):205–214CrossRefGoogle Scholar
  31. Munne-Bosch S, Penuelas J (2003) Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217(5):758–766CrossRefGoogle Scholar
  32. Nabity PD, Hengmoss TM, Higley LG (2006) Effects of insect herbivory on physiological and biochemical (oxidative enzyme) responses of the halophyte atriplex subspicata (chenopodiaceae). Environ Entomol 35(6):1677–1689CrossRefGoogle Scholar
  33. Nippert JB, Duursma RA, Marshall JD (2004) Seasonal variation in photosynthetic of capacity of montane conifers. Funct Ecol 18(6):876–886CrossRefGoogle Scholar
  34. Peschiutta ML, Bucci SJ, Scholz FG, Goldstein G (2016) Compensatory responses in plant-herbivore interactions: impacts of insects on leaf water relations. Acta Oecol 73:71–79CrossRefGoogle Scholar
  35. Salle A, Ye H, Yart A, Lieutier F (2008) Seasonal water stress and the resistance of Pinus yunnanensis to a bark-beetle-associated fungus. Tree Physiol 28(5):679–687CrossRefGoogle Scholar
  36. Scebba F, Arduini I, Ercoli L, Sebastiani L (2006) Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plant 50(2):688–692CrossRefGoogle Scholar
  37. Singh SK, Reddy VR, Fleisher DH, Timlin DJ (2017) Relationship between photosynthetic pigments and chlorophyll fluorescence in soybean under varying phosphorus nutrition at ambient and elevated CO2. Photosynthetica 55(3):421–433CrossRefGoogle Scholar
  38. Sivaci A, Elmas E, Bozkurt N, Duman S (2012) The effects of the pine sac beetle (thaumetopoea pityocampa Schiff.) on total phenolic compounds and photosynthetic pigment contents in pine species (Pinus nigra L. and Pinus brutia Ten.). Afr J Biotech 11(78):14297–14304CrossRefGoogle Scholar
  39. Sun J, Clarke SR, Kang L, Wang H (2005) Field trials of potential attractants and inhibitors for pine shoot beetles in the Yunnan province, China. Annu For Sci 62(1):9–12CrossRefGoogle Scholar
  40. Tan Y, Liang Z, Shao H, Du F (2006) Effect of water deficits on the activity of anti-oxidative enzymes and osmoregulation among three different genotypes of Radix Astragali at seeding stage. Colloids Surf B 49(1):60–65CrossRefGoogle Scholar
  41. Tao Z, Bo L (2012) Performance of Tomicus yunnanensis and Tomicus minor (Col., Scolytinae) on Pinus yunnanensis and Pinus armandii in Yunnan, Southwestern China. Psyche. CrossRefGoogle Scholar
  42. Tao Z, Zhou N, Li LS (2003) The reproduction biology of Tomicus piniperda in living Pinus yunnanensis. J Northwest For Univ 18:47–49Google Scholar
  43. Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of drought plants. Plant Cell Environ 16(4):341–349CrossRefGoogle Scholar
  44. Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62(1):1–9CrossRefGoogle Scholar
  45. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19(2):195–216PubMedGoogle Scholar
  46. Wang LY, Zhang HY, Zhu Y, Yu L, Cong B (2011) Physiological response of rice plants to Oulema oryzae feeding. Chin J Appl Entomol 48(4):928–933Google Scholar
  47. Wilson KB, Baldocchi DD, Hanson PJ (2000) Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf aging and drought in mature deciduous tree species. Tree Physiol 20(12):787CrossRefGoogle Scholar
  48. Ye H (1991) On the bionomy of Tomicus piniperda (L.) (Col., Scolytidae) in the Kunming region of China. J Appl Entomol 112(1–5):366–369Google Scholar
  49. Ye H (1996) Studies on the biology of Tomicus piniperda (Col., Scolytidae) in the shoot-feeding period. Acta Entomol Sin 39(1):58–62Google Scholar
  50. Ye H (1999) Studies on attacks by Tomicus piniperda (Col., Scolytidae) on Yunnan pine trees. Acta Entomol Sin 42(4):394–400Google Scholar
  51. Ye H, Li LS (1994) The distribution of Tomicus piniperda (L.) population in the crown of Yunnan pine during the shoot feeding period. Acta Entomol Sin 37:311–316Google Scholar
  52. Ye H, Zhimo Z (1995) Life table of Tomicus piniperda (L.) (Col., Scolytidae) and its analysis. J Appl Entomol 119(1–5):145–148Google Scholar
  53. Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H, Shigeoka S (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J 37(1):21–33CrossRefGoogle Scholar
  54. Zhou XD, Ye H, Ding HS (1999) On fungal flora inside egg galleries of Tomicus piniperda attacking Pinus yunnanensis. For Res 12(5):556–560Google Scholar

Copyright information

© Northeast Forestry University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Juan Liu
    • 1
    • 2
  • Hang Chen
    • 1
    • 2
  • Jianmin Wang
    • 1
    • 2
  • Xiaoming Chen
    • 1
    • 2
  • Zixiang Yang
    • 1
    • 2
  • Junsheng Liang
    • 2
    • 3
  1. 1.The Research Institute of Resource InsectsChinese Academy of ForestryKunmingPeople’s Republic of China
  2. 2.Key Laboratory of Breeding and Utilization of Resource Insects of State Forestry AdministrationKunmingPeople’s Republic of China
  3. 3.Hunan Academy of ForestryChangshaPeople’s Republic of China

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