Radial growth and non-structural carbohydrate partitioning response to resin tapping of slash pine (Pinus elliottii Engelm. var. elliottii)
Tóm tắt
Slash pine (Pinus elliottii Engelm. var. elliottii) is a resin-producing species grown worldwide for significant economic benefits for wood production. Resin tapping creates a carbon sink at the expense of carbon allocation for growth and consequently, wood production may be reduced. Non-structural carbohydrates comprising starch and sugars stored in plant organs, may serve as intermediate pools between assimilation and utilisation. However, the effect of resin tapping between tree growth and non-structural carbohydrates is not well understood. This study investigated (1) the effects of resin tapping on radial growth, (2) the effects of resin tapping on non-structural carbohydrate pools in different compartments, and (3) the feasibility of resin production without disruption of tree growth. Twenty one-year-old slash pines were subjected to resin tapping over two successive years. Non-structural carbohydrate concentrations in needles, branches, stem phloem, and roots of tapped and untapped trees in summer and winter were determined after the second year of resin harvest. The results showed that tapping had no significant effects on annual increments. Starch was the dominant non-structural carbohydrate fraction, regardless of tissues and season, and constituted up to 99% of the total non-structural carbohydrates in the phloem and roots. Glucose and fructose were the dominant sugars; sucrose was negligible. Compared with the controls, tapped trees showed 26% lower non-structural carbohydrate concentration in the phloem above the tapping wound in summer, which was attributable to the decreased abundance of starch, glucose, fructose, and sucrose. In winter, the altered non-structural carbohydrate profiles in the phloem above the tapping wounding were minimised as a result of recovery of the sugar concentrations. In contrast to free sugars, which accumulated substantially in needles and branches during winter, starch was enriched in the phloem, roots, and current-year needles. The results provide evidence for a localised effect of resin tapping, and highlight the observation that resin extraction does not always cause a sacrifice in wood growth under a moderate resin-tapping intensity in slash pine plantations.
Tài liệu tham khảo
Alfieri FJ, Evert RF (1968) Seasonal development of the secondary phloem in Pinus. Am J Bot 55(4):518–528
Allen SE (1974) Chemical analysis of ecological materials. J Appl Ecol 13(2):650–651
Bansal S, Germino MJ (2009) Temporal variation of nonstructural carbohydrates in montane conifers: similarities and differences among developmental stages, species and environmental conditions. Tree Physiol 29(4):559–568
Bonello P, Gordon TR, Herms DA, Wood DL, Erbilgin N (2006) Nature and ecological implications of pathogen-induced systemic resistance in conifers: a novel hypothesis. Physiol Mol Plant Pathol 68(4–6):95–104
Boschiero FA, Tomazzello-Filho M (2012) Anatomical aspects of resin canals and oleoresin production in pine trees. Biol Chem Appl 9–24
Chantuma P, Thanisawanyangkura S, Kasemsap P, Thaler P, Gohet E (2007) Increase in carbohydrate status in the wood and bark tissues of Hevea brasiliensis by double-cut alternative tapping system. Kasetsart J Nat Sci 41(41):442–450
Chantuma P, Lacointe A, Kasemsap P, Thanisawanyangkura S, Gohet E, Clément A, Guilliot A, Améglio T, Thaler P (2009) Carbohydrate storage in wood and bark of rubber trees submitted to different level of C demand induced by latex tapping. Tree Physiol 29(8):1021–1031
Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026
Chen F, Yuan YJ, Yu SL, Zhang TW (2016) Influence of climate warming and resin collection on the growth of Masson pine (Pinus massoniana) in a subtropical forest, southern China. Trees 30(3):1017–1017
Chong J, Soufan O, Li C, Caraus I, Li SZ, Bourque G, Wishart DS, Xia JG (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46(W1):W486–W494
Cown DJ, Donaldson LA, Downes GM (2011) A review of resin features in radiata pine. NZ J for Sci 41:41–60
Dickson RE (1989) Carbon and nitrogen allocation in trees. ANN for Sci 46(S):631s–647s
Du BG, Jansen K, Junker LV, Eiblmeier M, Kreuzwieser J, Gessler A, Ensminger I, Rennenberg H (2014) Elevated temperature differently affects foliar nitrogen partitioning in seedlings of diverse Douglas-fir provenances. Tree Physiol 34(10):1090–1101
Génova M, Caminero L, Dochao J (2014) Resin tapping in Pinus pinaster: effects on growth and response function to climate. Eur J for Res 133(2):323–333
Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20(6):1281–1328
Gholz HL, Cropper WPJ (1991) Carbohydrate dynamics in mature Pinus elliottii var. elliottii trees. Can J for Res 21(12):1742–1747
Gruber A, Pirkebner D, Florian C, Oberhuber W (2012) No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress. Plant Biol 14(1):142–148
Gruber A, Pirkebner D, Oberhuber W (2013) Seasonal dynamics of mobile carbohydrate pools in phloem and xylem of two alpine timberline conifers. Tree Physiol 33(10):1076–1083
Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosciences 30(5):761–776
Hansen J, Beck E (1994) Seasonal changes in the utilization and turnover of assimilation products in 8-year-old Scots pine (Pinus sylvestris L.) trees. Trees 8(4):172–182
Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytol 211:386–403
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67(3):283–335
Hesse PR (1971) A textbook of soil chemical analysis. John Murray Ltd, London, p 520
Hill AL, Whitehill JG, Opiyo SO, Phelan PL, Bonello P (2012) Nutritional attributes of ash (Fraxinus spp.) outer bark and phloem and their relationships to resistance against the emerald ash borer. Tree Physiol 32(12):1522–1532
Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26(7):1067–1081
Jacob JL, Prévôts JC, Lacote R, Gohet E, Clément A, Gallois R, Joet T, Pujade-Renaud V, D’Auzac J (1998) The biological mechanisms controlling Hevea brasiliensis rubber yield. Plant Res Dev 5:5–17
Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7(3):235–246
Kozlowski TT (1992) Carbohydrate sources and sinks in woody plants. Bot Review 58:107–222
Krokene P, Nagy NE (2012) Anatomical aspects of resin-based defences in pine. Pine Resin: Biol Chem Appl, 67–86
Lombardero MJ, Ayres MP, Lorio PL Jr, Ruel JJ (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3(4):329–339
Luchi N, Ma R, Capretti P, Bonello P (2005) Systemic induction of traumatic resin ducts and resin flow in Austrian pine by wounding and inoculation with Sphaeropsis sapinea and Diplodia scrobiculata. Planta 221(1):75–84
Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129(3):1003–1018
Mengistu T, Frank KJ, Anten N, Fetene M, Tadesse W, Bongers F (2012) Tapping and carbon balance of the frankincense tree. In: Tadesse W, Desalegn G, Yirgu A (eds) Forestry and forest products in Ethiopia: technologies and issues. Ethiopian Institute of Agricultural Research, Addis Ababa, Ethiopia, pp 169–181
Mengistu T, Sterck FJ, Fetene M, Bongers F (2013) Frankincense tapping reduces the carbohydrate storage of Boswellia trees. Tree Physiol 33(6):601–608
Moreira X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol 35(2):112–123
Muga MO, Kirinya CN, Kuria LG (1995) An assesment of resin tapping from Pinus caribaea trees grown in Kwale district. A report to the Chief Conservator of Forests, Forest Department. Kefri
Murugesan K, Jain SH, Mohan S, Nair SG (2011) Wood exudates: an overview on aromatic gums and resins. J Indian Acad Wood Sci 8(2):72–75
Nagy NE, Krokene P, Solheim H (2006) Anatomical-based defense responses of Scots pine (Pinus sylvestris) stems to two fungal pathogens. Tree Physiol 26(2):159–167
Nair B (2000) Sustainable utilization of gum and resin by improved tapping technique in some species. In: Harvesting of non-wood. Presented at the Joint FAO/ECE/ILO Committee on forest technology, management and training, Menemenizmir, Turkey, p 293
Novick KA, Katul GG, McCarthy HR, Oren R (2012) Increased resin flow in mature pine trees growing under elevated CO2 and moderate soil fertility. Tree Physiol 32(6):752–763
Papadopoulos AM (2013) Resin tapping history of an aleppo pine forest in Central Greece. Open for Sci J. https://doi.org/10.2174/1874398601306010050
Phillips MA, Croteau RB (1999) Resin-based defenses in conifers. Trends Plant Sci 4(5):184–190
Popp MP, Wilkinson RC, Jokela EJ, Harding RB, Phillips TW (1989) Effects of slash pine phloem nutrition on the reproductive performance of Ips calligraphus (Coleoptera: Scolytidae). Environ Entomol 18(5):795–799
Rijkers T, Ogbazghi W, Wessel M, Bongers F (2006) The effect of tapping for frankincense on sexual reproduction in Boswellia papyrifera. J Appl Ecol 43(6):1188–1195
Rodrigues KCS, Azevedo PCN, Sobreiro LE, Pelissari P, Fett-Neto AG (2008) Oleoresin yield of Pinus elliottii plantations in a subtropical climate: effect of tree diameter, wound shape and concentration of active adjuvants in resin stimulating paste. Ind Crop Prod 27(3):322–327
Rodrigues-Corrêa KCDS, de Lima JC, Fett-Neto AG (2012) Pine oleoresin: tapping green chemicals, biofuels, food protection, and carbon sequestration from multipurpose trees. Food Energy Secur 1(2):81–93
Rodríguez-García A, López R, Martín JA, Pinillos F, Gil L (2014) Resin yield in Pinus pinaster is related to tree dendrometry, stand density and tapping-induced systemic changes in xylem anatomy. For Ecol Manag 313:47–54
Rodríguez-García A, Martín JA, López R, Mutke S, Pinillos F, Gil L (2015) Influence of climate variables on resin yield and secretory structures in tapped Pinus pinaster Ait. in central Spain. Agr for Meteorol 202:83–93
Rodríguez-García A, Martín JA, López R, Sanz A, Gil L (2016) Effect of four tapping methods on anatomical traits and resin yield in Maritime pine (Pinus pinaster Ait.). Ind Crop Prod 86:143–154
Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars: Metabolism, sensing and abiotic stress: A complex network in the life of plants. Plant Signal Behav 4(5):388–393
Ruel JJ, Ayres MP, Lorio J (1998) Loblolly pine responds to mechanical wounding with increased resin flow. Can J for Res 28(4):596–602
Silpi U, Thaler P, Kasemsap P, Lacointe A, Chantuma A, Adam B, Gohet E, Thaniswanyankura S, Améglio T (2006) Effect of tapping activity on the dynamics of radial growth of Hevea brasiliensis trees. Tree Physiol 26(12):1579–1587
Silpi U, Lacointe A, Kasempsap P, Thanysawanyangkura S, Chantuma P, Gohet E, Musigamart N, Clément A, Améglio T, Thaler P (2007) Carbohydrate reserves as a competing sink: evidence from tapping rubber trees. Tree Physiol 27(6):881–889
Soerianegara I, Lemmens RHMJ (1993) Plant resources of South-east Asia No: 5 (1) Timber trees: major commercial timbers. Wageningen, Netherlands, pp 384–391
State Forestry Bureau of China (2007) Technical regulations of resin tapping (LY/T 1694–2007)
Sung SJ, Kormanik PP, Black CC (1996) Temporal and spatial aspects of root and stem sucrose metabolism in loblolly pine trees. Tree Physiol 16(11–12):1003–1008
Susaeta A, Peter GF, Hodges AW, Carter DR (2014) Oleoresin tapping of planted slash pine (Pinus elliottii Engelm. var. elliottii) adds value and management flexibility to landowners in the southern United States. Biomass Bioenergy 68:55–61
Ticktin T (2004) The ecological implications of harvesting non-timber forest products. J Appl Ecol 41(1):11–21
Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Annu Rev Plant Biol 39(2):689–724
Tümen I, Reunanen M (2010) A comparative study on turpentine oils of oleoresins of Pinus sylvestris L. from three districts of Denizli. Rec Nat Prod 4(4):224–229
Tuomi J, Niemelä P, Chapin FS, Bryant JP, Sirén S (1988) Defensive responses of trees in relation to their carbon/nutrient balance. Mechanisms of woody plant defenses against insects. Springer, New York, pp 57–72
van der Maaten E, Mehl A, Wilmking M, van der Maaten-Theunissen M (2017) Tapping the tree-ring archive for studying effects of resin extraction on the growth and climate sensitivity of Scots pine. For Ecosyst 4(003):167–173
Vannoppen A, Kint V, Ponette Q, Verheyen K, Muys B (2019) Tree species diversity impacts average radial growth of beech and oak trees in Belgium, not their long-term growth trend. For Ecosyst 6(1):1–12
Wen XS, Kuang YY, Shi MQ, Li HZ, Luo LS, Deng RL (2004) Biology of Hylobitelus xiaoi (Coleoptera: Curculionidae), a new pest of slash pine. Pinus Elliottii J Econ Entomol 97(6):1958–1964
Xia JG, Wishart DS (2016) Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinform. https://doi.org/10.1002/cpbi.11
Zhang S, Jiang J, Luan QF (2016) Genetic and correlation analysis of oleoresin chemical components in slash pine. Genet Mol Res. https://doi.org/10.4238/gmr.15038982