Sex-specific responses of Populus deltoides to defoliation

Li Shuxin, Yu Lei, Duan Baoli, Peng Shuming

Abstract


There has been an increasing interest in understanding the differential effects of sexual dimorphism on plant stress responses. However, there is no clear pattern in the responses of the sexes to defoliation. In this study, the effects of different severity of artificial defoliation on biomass production, total nonstructural carbohydrate (NSC) concentration, and photosynthetic rate (PN) of male and female Populus deltoides were examined. We used half and full defoliation to observe the differences between the sexes in three harvest dates (1 week, 4 weeks, and 8 weeks after treatments). We hypothesized that female and male P. deltoides compared with an undefoliated control would have compensatory growth in response to defoliation treatments. Results showed that half and full defoliation reduced the growth of both sexes. Following half defoliation, root growth was reduced, especially in males, at T2 (4 weeks after defoliation) and T3 (8 weeks after defoliation), while males showed an increase in height increment under the half defoliation compared with the nondefoliation treatments. By contrast, females were more negatively affected by defoliation than males in terms of biomass after 8 weeks. One week after defoliation, PN increased significantly in females and males under half defoliation (+30%, +32%, respectively) and full defoliation (+58%, +56%, respectively). However, 8 weeks after defoliation, there was little difference in PN between defoliated and undefoliated female cuttings. Increases in stomatal conductance (gs) and leaf nitrogen were observed under fully defoliated female and male cuttings. Moreover, males had less NSC concentrations following half defoliation compared with females. Our results indicate that leaf compensatory growth in male cuttings of P. deltoides was maintained by obtaining greater photosynthetic capacity, higher leaf nitrogen, and lower NSC concentration following half and full defoliation. Our results highlight that females suffered from greater negative effects than did males following half defoliation, but under full defoliation, the differences between both sexes were subtle.

Keywords


artificial defoliation; Populus deltoides; nonstructural carbohydrates; net photosynthetic rate; sexual differences

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References


May BM, Carlyle JC. Effect of defoliation associated with Essigella californica on growth of mid-rotation Pinus radiata. For Ecol Manage. 2003;183(1–3):297–312. https://doi.org/10.1016/S0378-1127(03)00111-7

Carnegie AJ, Matsuki M, Haugenc DA, Hurley BP, Ahumada R, Klasmer P, et al. Predicting the potential distribution of Sirex noctilio (Hymenoptera: Siricidae), a significant exotic pest of Pinus plantations. Ann For Sci. 2006;63(2):119–128. https://doi.org/10.1051/forest:2005104

Durán A, Gryzenhout M, Slippers B, Ahumada R, Rotella A, Flores F, et al. Phytophthora pinifolia spnov. associated with a serious needle disease of Pinus radiata in Chile. Plant Pathol. 2008;57(4):715–727. https://doi.org/10.1111/j.1365-3059.2008.01893.x

Ma ZF, Liu J, Zhang SQ, Chen WX, Yang SQ. Observed climate changes in southwest China during 1961–2010. Advances in Climate Change Research. 2013;4(1):30–40. https://doi.org/10.3724/SP.J.1248.2013.030

Logan JA, Régnière J, Powell JA. Assessing the impacts of global warming on forest pest dynamics. Frontiers in Ecology and Environment. 2003;1(3):130–137. https://doi.org/10.1890/1540-9295(2003)001[0130:ATIOGW]2.0.CO;2

Netherer S, Schopf A. Potential effects of climate change on insect herbivores in European forests – general aspects and the pine processionary moth as specific example. For Ecol Manage. 2010;259(4–5):831–838. https://doi.org/10.1016/j.foreco.2009.07.034

Jacquet JS, Bosc A, O’Grady AP, Jactel H. Pine growth response to processionary moth defoliation across stand chronosequence. For Ecol Manage. 2013;293(1):29–38. https://doi.org/10.1016/j.foreco.2012.12.003

Jean-Sébastien J, Alexandre B, Anthony OG, Hervé J. Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiol. 2014;34(4):367–376. https://doi.org/10.1093/treephys/tpu018

Wills AJ, Burbidge TE, Abbott I. Impact of repeated defoliation on jarrah (Eucalyptus marginata) saplings. Aust For. 2004;67(3):194–198. https://doi.org/10.1080/00049158.2004.10674934

Pinkard EA. Physiological and growth responses related to pattern and severity of pruning in young Eucalyptus globulus. For Ecol Manage. 2003;182(1–3):231–245. https://doi.org/10.1016/S0378-1127(03)00046-X

Pinkard EA, Beadle CL. A physiological approach to pruning. International Forestry Review. 2000;2(4):295–305.

Iqbal N, Masood A, Khan NA. Analyzing the significance of defoliation in growth, photosynthetic compensation and source–sink relations. Photosynthetica. 2012;50(2):161–170. https://doi.org/10.1007/s11099-012-0029-3

Collin P, Epron D, Alaoui-sosse B, Badot PM. Growth responses of common ash seedings (Fraxinus excelsior L.) to total and partial defoliation. Ann Bot. 2000;85:317–323. https://doi.org/10.1006/anbo.1999.1045

Haukioja E, Koricheva J. Tolerance to herbivory in woody vs. herbaceous plants. Evol Ecol. 2000;14:551–562. https://doi.org/10.1023/A:1011091606022

Eyles A, Smith D, Pinkard EA, Smith I, Corkrey R, Elms S, et al. Photosynthetic responses of field grown Pinus radiata trees to artificial and aphid-induced defoliation. Tree Physiol. 2011;31(6):592–603. https://doi.org/10.1093/treephys/tpr046

Dickson RE. Carbon and nitrogen allocation in trees. Ann For Sci. 1989;46(suppl):631S-647S. https://doi.org/10.1051/forest:198905ART0142

Krauss N, Hinrichs W, Witt I, Fromme P, Pritzkow W, Dauter Z, et al. Three-dimensional structure of system I of photosynthesis at 6 Å resolution. Nature. 1993;361:326–331. https://doi.org/10.1038/361326a0

Vanderklein DW, Reich PR. The effect of defoliation intensity and history on photosynthesis, growth and carbon reserves of two conifers with contrasting leaf lifespans and growth habits. New Phytol. 1999;144:121–132. https://doi.org/10.1046/j.1469-8137.1999.00496.x

Li M, Hoch G, Körner C. Source/sink removal affects mobile carbohydrates in Pinus cembra at the swiss treeline. Trees. 2002;16(4–5):331–337. https://doi.org/10.1007/s00468-002-0172-8

Hudgeons JL, Knutson AE, Heinz KM, Deloach CJ, Dudley TL, Pattison RR. Defoliation by introduced Diorhabda elongata leaf beetles (Coleoptera: Chrysomelidae) reduces carbohydrate reserves and regrowth of Tamarix (Tamaricaceae). Biol Control. 2007;43(2):213–221. https://doi.org/10.1016/j.biocontrol.2007.07.012

Palacio S, Paterson E, Sim A, Hester AJ, Millard P. Browsing affects intra-ring carbon allocation in species with contrasting wood anatomy. Tree Physiol. 2011;31(2):150–159. https://doi.org/10.1093/treephys/tpq110

Quentin AG, Beadle CL, O’Grady AP, Pinkard EA. Effects of partial defoliation on closed canopy Eucalyptus globulus Labilladiere: growth, biomass allocation and carbohydrates. For Ecol Manage. 2011;261(3):695–702. https://doi.org/10.1016/j.foreco.2010.11.028

Heyden FVD, Stock WD. Nonstructural carbohydrate allocation following different frequencies of simulated browsing in three semi-arid shrubs. Oecologia. 1995;102(2):238–245. https://doi.org/10.1007/BF00333256

Renner SS, Ricklefs RE. Dioecy and its correlates in the flowering plants. Am J Bot. 1995;82(5):596–606. https://doi.org/10.2307/2445418

Augustin S, Denux O, Castagneyrol B, Jactel H, Karlinski L, Kieliszewska-Rokicka B, et al. Insect herbivory response to Populus nigra genetic diversity. International Poplar Symposium, Orvieto. 2010. http://www.versailles-grignon.inra.fr

Xu X, Yang F, Xiao X, Zhang S, Korpelainen H, Li C. Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant Cell Environ. 2008;31(6):850–860. https://doi.org/10.1111/j.1365-3040.2008.01799.x

Zhang S, Jiang H, Zhao H, Korpelainen H, Li C. Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol. 2014;34(4):343–354. https://doi.org/10.1093/treephys/tpu025

Chen L, Zhang L, Tu L, Xu Z, Zhang J, Gao S. Sex-related differences in physiological and ultrastructural responses of Populus cathayana, to Ni toxicity. Acta Physiol Plant. 2014;36(7):1937–1946. https://doi.org/10.1007/s11738-014-1570-4

Lichtenthaler HK. Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 1987;148(34):350–382. https://doi.org/10.1016/0076-6879(87)48036-1

Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA Bioenergetics. 1989;975(3):384–394. https://doi.org/10.1016/S0005-2728(89)80347-0

Mitchell AK. Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol. 1998;18(11):749–757. https://doi.org/10.1093/treephys/18.11.749

Nelson DW, Sommers LE. Total carbon, organic carbon and organic matter. In Methods of Soil Analysis. Part 2 ed. Page, A.L. p. 199. Madison, WI: American Society of Agronomy. 1982.

Livingston NJ, Guy RD, Sun ZJ, Ethier GJ. The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white spruce (Picea glauca) seedlings. Plant Cell Environ. 1999;22(3):281–289. https://doi.org/10.1046/j.1365-3040.1999.00400.x

Yemm EW, Willis AJ. The estimation of carbohydrates in plant extracts by anthrone. Biochem J. 1954;57:508–514. https://doi.org/10.1042/bj0570508

Zhao HX, Xu X, Zhang YB. Nitrogen deposition limits photosynthetic response to elevated CO2 differentially in a dioecious species. Oecologia. 2011;165(1):41–54. https://doi.org/10.1007/s00442-010-1763-5

Murata T. Enzymic mechanism of starch breakdown in germinating rice seeds I. An analytical study. Plant Physiol. 1968;43(12):1899–1905. https://doi.org/10.1104/pp.43.12.1899

Chen Z, Kolb TE, Clancy KM. Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: bud burst phenology, photosynthetic compensation and growth rate. Tree Physiol. 2001;21:1159–1169. https://doi.org/10.1093/treephys/21.16.1159

Quentin AG, Pinkard EA, Beadle CL, Wardlaw TJ, O’Grady AP, Paterson S, et al. Do artificial and natural defoliation have similar effects on physiology of Eucalyptus globules Labill. Seedlings? Ann For Sci. 2010;67:203–203. https://doi.org/10.1051/forest/2009096

Wiley E, Huepenbecker S, Casper BB, Helliker BR. The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol. 2013;33(11):1216–1228. https://doi.org/10.1093/treephys/tpt093

Ourry A, Boucaud J, Salette J. Nitrogen mobilization from stubble and roots during regrowth of defoliated perennial Ryegrass. J Exp Bot. 1988;39:803–809. https://doi.org/10.1093/ixb/39.6.803

Zhao W, Chen SP, Lin GH. Compensatory growth responses to clipping defoliation in Leymus chinensis (Poaceae) under nutrient addition and water deficiency conditions. Plant Ecol. 2008;196:85–99. https://doi.org/10.1007/s11258-007-9336-3

Warren CR, Livingston NJ, Turpin D. Responses of gas exchange to reversible changes in whole plant transpiration rate in two conifer species. Tree Physiol. 2003;23(12):793–803. https://doi.org/10.1093/treephys/23.12.793

Tarrynl T, Aark AA, Charles RW. Increased photosynthesis following partial defoliation of field-grown Eucalyptus globulus seedlings is not caused by increased leaf nitrogen. Tree Physiol. 2007;27(10):1481–1492. https://doi.org/10.1093/treephys/27.10.1481

Eyles A, Pinkard EA, O’Grady AP, Corkrey R, Beadle C, Mohammed C. Recovery after defoliation in Eucalyptus globulus saplings: respiration and growth. Trees. 2016;30(5):1543–1555. https://doi.org/10.1007/s00468-016-1388-3

Lavigne MB, Little CA, Major JE. Increasing the sink:source balance enhances photosynthetic rate of 1-year-old balsam fir foliage by increasing allocation of mineral nutrients. Tree Physiol. 2001;21(7):417–426. https://doi.org/10.1093/treephys/21.7.417

Matthew JP, Christine HF. Sink regulation of photosynthesis. J Exp Bot. 2001;52:1383–1400. https://doi.org/10.1093/jexbot/52.360.1383

Stitt M. Fructose-2, 6-bisphosphate as a regulatory molecule in plants. Annu Rev Plant Biol. 1990;41:153–185. https://doi.org/10.1146/annurev.pp.41.060190.001101

Roberts J, Wallace JS, Pitman RM. Factors affecting stomatal conductance of bracken below a forest canopy. J Appl Ecol. 1994;21(2):643–655. https://doi.org/10.2307/2403435

Hart M, Hogg EH, Lieffers VJ. Enhanced water relations of residual foliage following defoliation in Populus tremuloides. Can J Bot. 2000;78(5):583–590. https://doi.org/10.1139/b00-032

Elfadl MA, Luukkanen O. Effect of pruning on Prosopis juliflora: considerations for tropical dryland agroforestry. J Arid Environ. 2003;53(4):441–455. https://doi.org/10.1006/jare.2002.1069

Striker GG, Insausti P, Grimoldi AA. Floodings effects on plants recovering from defoliation in Paspalum dilatetum and Lotus tenuis. Ann Bot. 2008;102:247–254. https://doi.org/10.1093/aob/mcn083

Handa IT, Körner C, Hattenschwiler S. A test of the tree-line carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology. 2005;86(5):1288–1300. https://doi.org/10.1890/04-0711

Rapley LP, Potts BM, Battaglia M, Patel VS, Allen GR. Longterm realised and projected growth impacts caused by autumn gum moth defoliation of 2-year-old Eucalyptus nitens plantation trees in Tasmania, Australia. For Ecol Manage. 2009;258(9):1896–1903. https://doi.org/10.1016/j.foreco.2009.06.036

Pinkard EA, Battaglia M, Mohammed CL. Defoliation and nitrogen effects on photosynthesis and growth of Eucalyptus globulus. Tree Physiol. 2007;27(7):1053–1063. https://doi.org/10.1093/treephys/27.7.1053

Pinkard EA, Eyles A, O’Grady AP. Are gas exchange responses to resource limitation and defoliation linked to source: sink relationships? Plant Cell Environ. 2011;34(10):1652–1665. https://doi.org/10.1111/j.1365-3040.2011.02361.x

Eyles A, Pinkard EA, Mohammed C. Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol. 2009;29(6):753–764. https://doi.org/10.1093/treephys/tpp014




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