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

Abstract

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.

Keywords

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

References

[1] Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA, 2009, 106(30): 12311-12316.

[2] Campos PS, Quartin V, Ramalho JC, Nunes MA. Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol, 2003, 160(3): 283-292.

[3] Chen DL, Zhang X, Jiang BF, Yu PW. Effects on the content of proteins of poplars damaged by Apriona germari (Hope). Biol Disaster Sci, 2012, 35(1): 85-89.

[4] David MR, Ursula MRV, Matthew HS, Sharon BG, Carl JB, Donald RO. 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, 2014, 226: 136-146.

[5] Duan Y, Kerdelhue C, Ye H, Lieutier F. 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, 2004, 93(5): 416-422.

[6] Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol, 2005, 167(2): 353-376.

[7] Genty B, Briantais JM, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta, 1989, 990(1): 87-92.

[8] Gill RS, Gupta AK, Taggar GK, Taggar MS. Role of oxidative enzymes in plant defenses against insect herbivory. Acta Phytopathol Entomol Hung, 2010, 45(2): 277-290.

[9] Glenn EP, Nagler PL, Morino K, Hultine KR. Phreatophytes under stress: transpiration and stomatal conductance of saltcedar (Tamarix, spp.) in a high-salinity environment. Plant Soil, 2013, 371(1–2): 655-672.

[10] Golan K, Rubinowska K, Gorskadrabik E. Physiological and biochemical responses of Fern Nephrolepis Biserrata (Sw.) Schott. To Coccus Hesperidum L. infestation. Acta Biol Crac, 2013, 55(1): 93-98.

[11] Golan K, Rubinowska K, Kmieć K, Kot I, Górska-Drabik E, Łagowska B, Michałek W. Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species. Arthropod Plant Interact, 2015, 9(1): 55-65.

[12] Hahlbrock K, Bednarek P, Ciolkowski I, Hamberger B, Heise A, Liedgens H, Logemann E, Nurnberger T, Schmelzer E, Somssich IE, Tan J. Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proc Natl Acad Sci USA, 2003, 100(2): 14569-14576.

[13] Hermsmeier D, Schittko U, Baldwin IT. 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, 2001, 125: 683-700.

[14] Hofstetter RW, Mahfouz JB, Klepzig KD, Ayres MP. Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. J Chem Ecol, 2005, 31(3): 539-560.

[15] Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science, 2005, 307: 433-436.

[16] Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol, 2008, 59: 41-66.

[17] Huang W, Jia ZK, Han QF. Effects of herbivore stress by Aphis medicaginis Koch on the Malondialdehyde contents and activities of protective enzymes in different alfalfa varieties. Acta Ecol Sin, 2007, 27(5): 2177-2183.

[18] Jones HG. Partitioning stomatal and non-stomatal limitations to photosynthesis. Plant Cell Environ, 1985, 8(2): 95-104.

[19] Kessler A, Baldwin IT. Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol, 2002, 53: 299-328.

[20] Kirkendall LR, Faccoli M, Ye H. 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, 2008, 1819: 25-39.

[21] Li LS, Wang HL, Chai XS, Wang YX, Shu NB, Yang DS. Study on the biological characteristics of Tomicus yunnanensis and its damage. For Res, 1993, 6: 14-20.

[22] Li HS, Sun Q, Zhao SJ. Principles and techniques of plant physiological biochemical experiment, 2000 1 Beijing: Higher education press 134 138

[23] Li LM, Men XY, Ye BH, Yu Y, Zhang AS, Li LL, Zhou XH, Zhuang QY. Defense enxyme activity of Winter Jujube at different stages induced by the damage of Apolygus lucorum. Sci Agric Sin, 2014, 47(1): 191-198.

[24] Lieutier F, Yart A, Salle A. Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci, 2009 66 8 810

[25] Liu XP, Ge F, Chen CP, Wang GH, Li ZY. Progress in induced resistance of pines. Sci Silvae Sin, 2003, 39(5): 119-128.

[26] Liu YQ, Sun XY, Wang Y, Liu Y. Effects of shades on the photosynthetic characteristics and chlorophyll fluorescence parameters of Urtica dioica. Acts Ecol Sin, 2007, 27(8): 3457-3464.

[27] Liu Z, Chen W, He X. Cadmium-induced changes in growth and antioxidative mechanisms of a medicine plant (Lonicera japonica Thunb.). J Med Plants Res, 2011, 5(8): 1411-1417.

[28] Lu RC, Wang HB, Zhang Z, Byers JA, Jin YJ, Wen HF, Shi WJ. Coexistence and competition between Tomicus yunnanensis and T. minor (Coleoptera: Scolytinae) in Yunnan pine. Psyche, 2012, DOI:10: 1155/2012/185312.

[29] Mitra S, Baldwin IT. Independently silencing two photosynthetic proteins in Nicotiana attenuata has different effects on herbivore resistance. Plant Physiol, 2008, 148(2): 1128-1138.

[30] Miyashita K, Tanakamaru S, Maitani T, Kimura K. Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ Exp Bot, 2005, 53(2): 205-214.

[31] Munne-Bosch S, Penuelas J. Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta, 2003, 217(5): 758-766.

[32] Nabity PD, Hengmoss TM, Higley LG. Effects of insect herbivory on physiological and biochemical (oxidative enzyme) responses of the halophyte atriplex subspicata (chenopodiaceae). Environ Entomol, 2006, 35(6): 1677-1689.

[33] Nippert JB, Duursma RA, Marshall JD. Seasonal variation in photosynthetic of capacity of montane conifers. Funct Ecol, 2004, 18(6): 876-886.

[34] Peschiutta ML, Bucci SJ, Scholz FG, Goldstein G. Compensatory responses in plant-herbivore interactions: impacts of insects on leaf water relations. Acta Oecol, 2016, 73: 71-79.

[35] Salle A, Ye H, Yart A, Lieutier F. Seasonal water stress and the resistance of Pinus yunnanensis to a bark-beetle-associated fungus. Tree Physiol, 2008, 28(5): 679-687.

[36] Scebba F, Arduini I, Ercoli L, Sebastiani L. Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol Plant, 2006, 50(2): 688-692.

[37] Singh SK, Reddy VR, Fleisher DH, Timlin DJ. Relationship between photosynthetic pigments and chlorophyll fluorescence in soybean under varying phosphorus nutrition at ambient and elevated CO₂. Photosynthetica, 2017, 55(3): 421-433.

[38] Sivaci A, Elmas E, Bozkurt N, Duman S. 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, 2012, 11(78): 14297-14304.

[39] Sun J, Clarke SR, Kang L, Wang H. Field trials of potential attractants and inhibitors for pine shoot beetles in the Yunnan province, China. Annu For Sci, 2005, 62(1): 9-12.

[40] Tan Y, Liang Z, Shao H, Du F. 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, 2006, 49(1): 60-65.

[41] Tao Z, Bo L. Performance of Tomicus yunnanensis and Tomicus minor (Col., Scolytinae) on Pinus yunnanensis and Pinus armandii in Yunnan, Southwestern China. Psyche, 2012

[42] Tao Z, Zhou N, Li LS. The reproduction biology of Tomicus piniperda in living Pinus yunnanensis. J Northwest For Univ, 2003, 18: 47-49.

[43] Tardieu F, Davies WJ. Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of drought plants. Plant Cell Environ, 1993, 16(4): 341-349.

[44] Tuna AL, Kaya C, Dikilitas M, Higgs D. 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, 2008, 62(1): 1-9.

[45] Walling LL. The myriad plant responses to herbivores. J Plant Growth Regul, 2000, 19(2): 195-216.

[46] Wang LY, Zhang HY, Zhu Y, Yu L, Cong B. Physiological response of rice plants to Oulema oryzae feeding. Chin J Appl Entomol, 2011, 48(4): 928-933.

[47] Wilson KB, Baldocchi DD, Hanson PJ. Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf aging and drought in mature deciduous tree species. Tree Physiol, 2000 20 12 787

[48] Ye H. On the bionomy of Tomicus piniperda (L.) (Col., Scolytidae) in the Kunming region of China. J Appl Entomol, 1991, 112(1–5): 366-369.

[49] Ye H. Studies on the biology of Tomicus piniperda (Col., Scolytidae) in the shoot-feeding period. Acta Entomol Sin, 1996, 39(1): 58-62.

[50] Ye H. Studies on attacks by Tomicus piniperda (Col., Scolytidae) on Yunnan pine trees. Acta Entomol Sin, 1999, 42(4): 394-400.

[51] Ye H, Li LS. The distribution of Tomicus piniperda (L.) population in the crown of Yunnan pine during the shoot feeding period. Acta Entomol Sin, 1994, 37: 311-316.

[52] Ye H, Zhimo Z. Life table of Tomicus piniperda (L.) (Col., Scolytidae) and its analysis. J Appl Entomol, 1995, 119(1–5): 145-148.

[53] Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H, Shigeoka S. Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J, 2004, 37(1): 21-33.

[54] Zhou XD, Ye H, Ding HS. On fungal flora inside egg galleries of Tomicus piniperda attacking Pinus yunnanensis. For Res, 1999, 12(5): 556-560.