Thermal acclimation of photosynthesis and respiration in Pinus radiata and Populus deltoides to changing environmental conditions

Transcription

1 Therml cclimtion of photosynthesis nd respirtion in Pinus rdit nd Populus deltoides to chnging environmentl conditions A thesis sumitted in fulfilment of the requirement for the Degree of Doctor of Philosophy in Plnt Physiology t the University of Cnterury y Li Fern, Genevieve Ow 2008

2 This thesis is dedicted to my prents who hve een so supportive ll this time The work presented in this thesis is, to the est of my knowledge nd elief, originl. The mteril hs not een sumitted, either in whole or in prt, for degree t this or ny other University. Li Fern Ow June 2008 i

3 CONTENTS CONTENTS.. ii LIST OF TABLES vi LIST OF FIGURES... vii LIST OF ABBREVIATIONS x ABSTRACT.. 1 CHAPTER 1. 4 INTRODUCTION, REVIEW OF LITERATURE AND RATIONALE INTRODUCTION REVIEW OF LITERATURE Photosynthesis Photosynthesis in evergreen species Photosynthesis in deciduous species The role of lef ge in photosynthesis Photosynthetic cclimtion Lef ge nd its effects on photosynthetic cclimtion Respirtion Respirtory cclimtion Mechnisms of cclimtion The role of lef ge in respirtion Emerging role of the lterntive oxidse (AOX) pthwy in respirtion Respirtion / photosynthetic (R/P) rtio Plnt respirtion in wrmer world The importnce of nitrogen Nitrogen (N) nd photosynthetic cclimtion Nitrogen (N) nd respirtory cclimtion Modelling of plnt cron fluxes RATIONALE OF THE PRESENT STUDY SIMPLIFIED SCHEMATIC ILLUSTRATION BOTANICAL DESCRIPTION OF STUDY SPECIES ii

4 1.5.1 Pinus rdit Populus deltoides OVERVIEW. 38 CHAPTER Therml cclimtion of lef respirtion ut not photosynthesis in Populus deltoides x nigr. 2.1 INTRODUCTION MATERIALS AND METHODS Growth conditions nd experimentl design Mesurements of respirtion, photosynthesis nd lef chrcteristics Sttisticl nlysis RESULTS Folir chrcteristics Photosynthesis Respirtion DISCUSSION Photosynthetic response to chnges in growth temperture Respirtory responses to chnges in growth temperture Blnce etween photosynthesis nd respirtion SUMMARY.. 68 CHAPTER Therml cclimtion of respirtion ut not photosynthesis in Pinus rdit INTRODUCTION MATERIALS AND METHODS Plnt mteril nd environmentl conditions Gs exchnge mesurements Oxygen electrode mesurements Sttisticl nlysis RESULTS Needle chrcteristics Photosynthesis. 81 iii

5 3.3.3 Respirtion Enzymtic ctivity of the cytochrome nd lterntive oxidse pthwys DISCUSSION Photosynthetic response to temperture trnsfer Respirtory responses to chnges in temperture Blnce etween photosynthesis nd respirtion SUMMARY.. 98 CHAPTER Sesonl vrition in folir cron exchnge in Pinus rdit nd Populus deltoides: respirtion cclimtes fully to chnges in temperture ut photosynthesis does not 4.1 INTRODUCTION MATERIALS AND METHODS Site description Gs exchnge mesurements nd tissue nlysis Dt nlysis RESULTS Folir chrcteristics Photosynthesis Respirtion DISCUSSION Response of photosynthesis to temperture Response of respirtion to temperture Blnce etween respirtion nd photosynthesis SUMMARY CHAPTER Modelling the responses of folir cron exchnge in Pinus rdit nd Populus deltoides INTRODUCTION MATERIALS AND METHODS Modelling cclimtion of photosynthesis nd respirtion RESULTS Modelling of net cron exchnge iv

6 5.3.2 The impct of cclimtion on nnul lef respirtion DISCUSSION Temperture cclimtion of drk respirtion SUMMARY CHAPTER Generl discussion nd conclusions DIAGRAMMATIC ILLUSTRATION OF PRINCIPAL FINDINGS DISCUSSION OF PRINCIPAL FINDINGS Respirtory cclimtion to temperture Mechnisms underpinning respirtory cclimtion Temperture response of photosynthesis THE IMPACT OF FOLIAR PROPERTIES Nitrogen Crohydrtes Respirtory enzymtic chrcteristics Modelling of plnt cron fluxes FURTHER STUDIES Chllenge of testing plnt responses to temperture Process-sed models nd mechnistic chnges underpinning the cclimtion response of respirtion Response of photosynthesis to temperture Concluding sttement ACKNOWLEDGEMENTS REFERENCES APPENDIX v

7 LIST OF TABLES CHAPTER 2 Tle 2.1 Rte of lef respirtion in Populus deltoides x nigr plnts trnsferred etween vrious growth tempertures. 56 Tle 2.2 Activity of the cytochrome (COX) nd lterntive oxidse (AOX) pthwys in Populus deltoides x nigr plnts trnsferred etween vrious growth tempertures 61 CHAPTER 3 Tle 3.1 Specific lef re (S m 2 kg -1 ) nd nitrogen content per unit lef re (N g m -2 ) in pre-existing nd new needles for Pinus rdit plnts trnsferred etween vrious growth tempertures.. 82 Tle 3.2 Activity of the cytochrome (COX) nd lterntive oxidse (AOX) pthwys in Pinus rdit plnts trnsferred etween vrious growth tempertures CHAPTER 4 Tle 4.1 Significnt regressions in figure 4.4 re descried y the following equtions Tle 4.2 Prmeters descriing the temperture response of V cmx nd J mx. 121 CHAPTER 5 Tle 5.1 Annul simultion of drk respirtion nd net photosynthesis of Pinus rdit nd Populus deltoides sed on dt generted from growth chmer experiments 135 Tle 5.2 Simulted monthly net photosynthesis of Pinus rdit nd Populus deltoides over 12 nd 7-month period respectively CHAPTER 6 Tle 6.1 Prmeters descriing the temperture response of V cmx nd J mx in the current s well s in previous studies vi

8 LIST OF FIGURES CHAPTER 1 Fig. 1.1 Simplified schemtic illustrtion of n investigtion into the potentil of photosynthetic nd respirtory cclimtion under field nd controlled environmentl conditions.. 35 Fig. 1.2 Leves of Pinus rdit nd Populus deltoides two species used in this reserch CHAPTER 2 Fig. 2.1 Vrition in folir nitrogen concentrtion nd specific lef re in Populus deltoides nigr plnts under three temperture trnsfer regimes Fig. 2.2 Photosynthetic prmeters in Populus deltoides nigr plnts under three temperture trnsfer regimes Fig. 2.3 Temperture response of Amx, Vcmx nd Rd/Amx t three dytime growth tempertures for Populus deltoides nigr plnts efore nd following trnsfer etween three temperture regimes. 58 Fig. 2.4 Instntneous nd cclimted responses of respirtion to temperture in Populus deltoides nigr 59 Fig. 2.5 Temperture response prmeters of drk respirtion (R 10 nd Q 10 ) under three temperture trnsfer regimes in Populus deltoides nigr.. 60 CHAPTER 3 Fig. 3.1 Photosynthetic prmeters in Pinus rdit plnts under three temperture trnsfer regimes Fig. 3.2 Photosynthetic temperture response of V cmx nd J mx t three dy-time growth tempertures for Pinus rdit plnts Fig. 3.3 Instntneous nd cclimted responses of respirtion to temperture in Pinus rdit vii

9 Fig. 3.4 Temperture response prmeters of drk respirtion (R 10, Q 10 nd R d /A mx ) under three temperture trnsfer regimes in Pinus rdit. 88 Fig. 3.5 Rtios of needle R in drkness (R drk ) to light sturted photosynthesis t mient CO 2 (A mx ) t three night-time growth tempertures for Pinus rdit plnts.. 89 CHAPTER 4 Fig. 4.1 Sesonl vrition in specific lef re, nitrogen, solule sugr nd strch concentrtion in field-grown trees of Pinus rdit nd Populus deltoides s function of time 109 Fig. 4.2 Photosynthetic prmeters clculted from A/C i nd A/Q responses in Pinus rdit nd Populus deltoides grown in the field nd stomtl limittion on the rte of photosynthesis s function of time. 111 Fig. 4.3 Temperture responses J mx nd V cmx t mximum dytime growth tempertures for Pinus rdit nd Populus deltoids. 113 Fig. 4.4 The reltionship etween V cmx, J mx, R 10, Q 10 nd re-sed lef nitrogen, sugr nd strch concentrtions in leves of Pinus rdit nd Populus deltoides smpled over 12-month period 114 Fig. 4.5 Temperture response prmeters of drk respirtion (R 10 nd Q 10 ) in Pinus rdit nd Populus deltoides smpled over different sesons. 115 Fig. 4.6 Are-sed drk respirtion rte nd the Q 10 of lef respirtion in reltion to the 3- dy minimum temperture verge in Pinus rdit nd Populus deltoides smpled over different sesons 117 Fig. 4.7 Correltion coefficients of R 10 nd Q 10 of Pinus rdit nd Populus deltoides plotted s function of the time window (dys) used to clculte preceding verge mient temperture 118 Fig. 4.8 Long term (cclimted) respirtion rte of pine nd poplr s function of temperture 118 Fig. 4.9 Rtio of respirtion in drkness (R drk ) to light sturted photosynthesis t mient CO 2 (A mx ) in Pinus rdit nd Populus deltoides smpled over different sesons 119 viii

10 CHAPTER 5 Fig. 5.1 Model of R drk s function of temperture in the short nd longer term 131 Fig. 5.2 Model simultion of lef drk respirtion of pine nd poplr (growth chmer dt) over one-yer period Fig. 5.3 Simulted monthly totl lef drk respirtion over 12 nd 7-month period etween 2005 to 2006 for pine nd poplr 139 CHAPTER 6 Fig. 6.1 Digrm showing the cclimtion potentil of photosynthesis nd respirtion in pre-existing nd new tissues s well s chnges in respirtory enzymtic properties under chnging temperture conditions Fig. 6.2 Digrm showing the cclimtion potentil of photosynthesis nd respirtion in two contrsting tree species s well s the regultion of folir properties on key metolic processes exposed to sesonl chnges. 149 ix

11 LIST OF ABBREVIATIONS A A mx ANOVA AOX ATP C C i CCCP COX CV E 0 GCM Gt HN J mx K KCN kp LN L stom photosynthesis mximum photosynthetic rte t sturting light nlysis of vrince lterntive oxidse denosine triphosphte tmospheric CO 2 concentrtion intercellulr CO 2 concentrtion cronylcynide m-chlorophenylhydrzone cytochrome oxidse coefficient of vrition ctivtion energy of respirtion glol cron cycle models gigtons high nitrogen plnts mximum photosynthetic electron trnsport rte kelvin potssium cynide kilopscl low nitrogen plnts reltive stomtl limittion on photosynthesis x

12 MAF N N re N mss Ministry of Agriculture nd Forestry nitrogen nitrogen on n re sis nitrogen on mss sis 18 O oxygen-18, stle isotope P PFD Pg P i PnET PNUE Q Q 10 R 10 Rd R/P RuBP SE SHAM SLA T T vg pscl photosynthetic photon flux density petgrms phosphte supply net primry productivity ecosystem model photosynthetic nitrogen utilistion efficiency irrdince The temperture coefficient - mesure of the rte of chnge of iologicl or chemicl system s consequence of incresing the temperture y 10 C respirtion rte t reference temperture of 10 o C drk respirtion rte respirtion/photosynthesis rtio riulose-1,5-isphosphte stndrd error of the men slicylhydroxmic cid specific lef re temperture temperture verge xi

13 TCA T opt V cmx tricroxylic cid cycle optimum temperture mximum croxyltion rte of riulose 1.5-isphosphte xii

14 ABSTRACT Although it hs long een recognized tht physiologicl cclimtion of photosynthesis nd respirtion cn occur in plnts exposed to chnging environmentl conditions (e.g. light, temperture or stress), the extent of cclimtion in different tissues (i.e. pre-existing nd new folige) however, hs not received much ttention until recently. Furthermore, few studies hve investigted the extent of photosynthetic nd respirtory cclimtion under nturl conditions, where ir tempertures vry diurnlly nd sesonlly. In this study, the effects of vritions in temperture on respirtory CO 2 loss nd photosynthetic cron ssimiltion were exmined under oth controlled nd nturl environments. The purpose of the investigtions descried in this thesis ws to identify the effects cclimtion would hve on two key metolic processes in plnts exposed to temperture chnge, with emphsis lso plced on the role of nutrition (nitrogen) nd respirtory enzymtic chrcteristics on the potentil for cclimtion in two contrsting tree species, Pinus rdit nd Populus deltoides. Controlled-environment studies (Chpter 2 nd 3) estlished tht rtes of folir respirtion re sensitive to short-term chnges in temperture (incresing exponentilly with temperture) ut in the longer-term (dys to weeks), folir respirtion cclimtes to temperture chnge. As result, rtes of drk respirtion mesured t ny given temperture re higher in cold-cclimted nd lower in wrm-cclimted plnts thn 1

15 Astrct would e predicted from n instntneous response. Acclimtion in new folige (formed under the new temperture environment) ws found to result in respirtory homeostsis (i.e. constnt rtes of folir respirtion following long-term chnges in temperture, when respirtion is mesured t the previling growth temperture). Aville evidence suggests tht sustntil djustments in folir respirtion tend to e developmentlly dependent. This my in prt explin why respirtory homeostsis ws only oserved in new ut not in pre-existing tissues. Step chnges in temperture (cold nd wrm trnsfers) resulted in significnt chnges in photosynthetic cpcity. However, in strk contrst to the findings of respirtion, there ws little evidence for photosynthetic cclimtion to temperture chnge. The results otined from field studies (Chpter 4) show tht in the long-term over full yer, drk respirtion rtes in oth tree species were insensitive to temperture ut photosynthesis retined its sensitivity, incresing with incresing temperture. Respirtion in oth species showed significnt downregultion during spring nd summer nd increses in respirtory cpcity were oserved in utumn nd winter. Therml cclimtion of respirtion ws ssocited with chnge in the concentrtion of solule sugrs. Hence, cclimtion of drk respirtion under nturlly chnging environment is chrcterized y chnges in the temperture sensitivity nd pprent cpcity of the respirtory pprtus. The results from controlled nd nturl-environment studies were used to drive leflevel model (which ccounted for drk respirtory cclimtion) with the im of 2

16 Astrct forecsting the overll impct of responses of photosynthesis nd respirtion in the long term (Chpter 5). Modellers utilise the temperture responses of photosynthesis nd respirtion to prmeterize cron exchnge models ut often ignore cclimtion nd use only instntneous responses to drive such models. The studies here hve shown tht this cn result in erroneous estimtes of cron exchnge s strong respirtory cclimtion occurs over longer periods of temperture chnge. For exmple, it ws found here tht the filure to fctor for drk respirtory cclimtion resulted in the underestimtion of cron losses y folir respirtion during cooler months nd n overestimtion during wrmer months - such discrepncies re likely to hve n importnt impct on determintions of the cron economy of forests nd ecosystems. The overll results sustntite the conclusion tht understnding the effect of vritions in temperture on rtes of cron loss y plnt respirtion is prerequisite for predicting estimtes of tmospheric CO 2 relese in chnging glol environment. It hs een shown here tht within moderte rnge of tempertures, rte of cron uptke y photosynthesis exceeds the rte of cron loss y plnt respirtion in response to wrming s result of strong respirtory cclimtion to temperture chnge. This hs strong implictions for models which fil to ccount for cclimtion of respirtion. At present, respirtion is ssumed to increse with incresing tempertures. This erroneous ssumption supports conclusions linking wrming to the reinforcement of the greenhouse effect. 3

17 Chpter 1 Introduction, review of literture nd rtionle 1.1 Introduction The recent upwrd trend in glol verge tempertures egn in the 1970s with incresingly pronounced wrming occurring towrds the end of the 20 th century. The 1990s represented the wrmest decde of the millennium, with 1998 the wrmest yer in tht period (IPCC 2007). Hence, it is pprent tht we live in period of glol wrming. The underlying cuse of this wrming trend is generlly ccepted to e the nthropogenic emission of greenhouse gses which re responsile for the re-emission of long-wve rdition ck to the erth s surfce (the greenhouse effect ). The most prevlent greenhouse gs is CO 2, which is lso the sic sustrte for photosynthesis nd thus the rw mteril for plnt growth. Approximtely hlf of ll iomss consists of cron. Therefore, plnt growth nd the glol cron cycle, which ultimtely determines tmospheric concentrtion of CO 2, re inextricly linked. Anthropogenic emissions of CO 2 re currently rising rpidly, with 7.0 Pg C yer -1 coming from fossil fuel urning nd cement-mking (Morison nd Morecroft 2006), nd further 1-2 Pg C yer -1 from deforesttion (IPCC 2007). Approximtely 3 Pg of cron remins 4

18 Chpter 1 in the tmosphere s CO 2, where its concentrtion is incresing t rte of 1-2 ppm y volume ech yer (Ainsworth nd Long 2005). The reminder is dissolved in the ocen or tken up y terrestril vegettion (Aer et l. 2001). Since plnts re orgnisms whose ody temperture vries with the temperture of their immedite environment, nd since they commonly cnnot move, except through reproduction, physiologicl cclimtion of plnt process (e.g. photosynthesis nd respirtion) re used to cope with chnging environmentl conditions. Although plnts re unle to escpe the different environmentl perturtions they experience, they hve evolved vriety of mechnisms tht reduce the direct impct of chnging tempertures on plnt growth nd development. Hence, extensive reserch hs een devoted to the study of the effects of environmentl fctors on plnt growth nd metolism. In terms of plnt response to the environment three spects re of importnce: (1) short-term responses, (2) cclimtion to new environmentl conditions, nd (3) survivl. Ech of these requires very different metolic nd regultory responses. It is often ssumed tht tmospheric wrming enhnces respirtory cron losses, cusing ecosystem or forest C-stocks to deplete (Wlther et l. 2001). However, this is n oversimplistic ssumption derived from the instntneous temperture responses of ctive tissues. Long-term glol wrming should not e confused with short-term wrming. Given sufficient time the initil effects of n increse in temperture my well e significntly reduced in mgnitude, vi processes of therml cclimtion. The purpose of the investigtion descried in this thesis ws to ssess the effects of chnging mient tempertures nd vrile levels of nutrition (nitrogen) on physiologicl nd enzymtic 5

19 Chpter 1 processes underpinning respirtion nd photosynthesis nd their potentil to cclimte in two contrsting tree species, Pinus rdit nd Populus deltoides. 1.2 Review of literture This review dels primrily with the cclimtion potentil of two min metolic processes in plnts, respirtion nd photosynthesis. The study of ech individul component is not sufficient to comprehend the effects of temperture chnge on plnt cron lnce s oth processes re closely coupled. Emphsis is lso given to the role of nitrogen nd enzymtic processes ssocited with the process of respirtory nd photosynthetic cclimtion Photosynthesis Photosynthesis is the primry physiologicl process responsile for plnt cron cquisition. Effects of environmentl fctors nd stressful conditions on lef photosynthesis (CO 2 ssimiltion) hve een reltively well studied. Here I focus on the effects of temperture chnge on plnt photosynthesis. Typiclly, photosynthesis is gered to n optimum temperture which not only vries with species ut is different for different component processes (Berry nd Bjorkmn 1980). Aove nd elow the optimum temperture, photosynthesis is less efficient. Trditionlly, the decrese in plnt growth t high tempertures is ttriuted to higher optimum temperture for respirtion thn for photosynthesis, thus decresing the dily net cron gined. Reserch in recent yers hs confirmed this ide through oservtions of rtes of photosynthesis tht often decrese shrply t tempertures ove the optimum vlue. At this point the lnce 6

20 Chpter 1 etween CO 2 fixtion nd CO 2 relese shifts in fvour of relese, ecuse (1) the ffinity of ruisco for CO 2 declines, (2) the cpcity of ruisco ctivse required to mintin ruisco in n ctivted stte declines to limiting levels (3) electron trnsport ecomes limiting to photosynthesis (Ymori et l. 2005). In contrst, drk respirtion stedily (exponentilly) increses with temperture until the rte decreses rpidly ner the lethl het limit (Morison nd Morecroft 2006). This difference in the temperture responses of photosynthesis nd respirtion is the sis for the notion tht greenhouse wrming will led to shift in the lnce etween photosynthesis nd respirtion in fvour of cron relese. However, current environmentl conditions pper more fvourle for photosynthesis over respirtion. Recent studies show tht photosynthesis exceeds respirtion on glol scle owing to the presence of green, growing plnts exerting positive cron lnce (Grce nd Zhng 2006). Additionlly, three forms of chnges in the environment lso exert positive effect on photosynthesis (Lwlor 1987). These re (1) moderte increse in CO 2, which stimultes photosynthesis (2) wrming in res tht re currently too cold for photosynthesis nd (3) the deposition of nthropogenic nitrogen s mmonium or nitrte cting s fertiliser, which enhnces photosynthesis Photosynthesis in evergreen species The lef model of photosynthesis presented y Frquhr et l. (1980) ssumes tht photosynthesis is primrily limited y the slower of two processes (1) the mximum rte of ruisco-ctlysed croxyltion nd (2) or the regenertion of riulose-1,5- isphosphte (RuBP) controlled vi the electron trnsport rte (RuBP-Limited). This model hs een used extensively for scling cron uptke to cnopies, ecosystems nd 7

21 Chpter 1 the iosphere. Furthermore, photosynthesis is temperture sensitive nd this hs een illustrted in recent studies (Monson et l. 2002; Monson et l. 2005; Zrter et l. 2006) which hve found tht photosynthesis is highly responsive to dy-to-dy environmentl chnges s well s sesonl chnges. However, evergreen species differ from deciduous species ecuse they must respond to nnul sesonl cycles tht trigger metolic events leding to cclimtion, nd thus must hve the genetic potentil to tolerte climtic extremes for their entire life cycle in order to survive. Therefore, evergreen leves tend to exhiit lower rtes of light-sturted photosynthesis nd experience environmentl/sesonl chnges in photosynthetic cpcity more grdully thn do leves of deciduous species. For exmple, recent reports (Mkel et l. 2004; Misson et l. 2006) hve shown tht the rte of photosynthesis in evergreens vries with seson. However, others hve reported little sesonlity in photosynthetic prmeters in evergreens (Dmesin et l. 1998; Emus et l. 1999; Wrren & Adms, 2004). Nonetheless, the reduction in photosynthetic rtes oserved during colder months hs een ttriuted to low tempertures which limit photosynthesis y slowing the rte t which metolic rections occur. The cesstion of growth in winter gretly reduces sink demnd for the products of photosynthesis nd thus induces photosynthetic downregultion (Adms et l. 2002; Adms et l. 2004). In summer, increses in photosynthesis hve een ttriuted to greter sink demnd (Turnull et l. 2002) Photosynthesis in deciduous species Unlike evergreen species, phenologicl limittions in deciduous species enforce gret sesonlity in photosynthetic prmeters (Wilson et l. 2000; Rokowski et l. 2002; 8

22 Chpter 1 Kosugi et l. 2003; Xu nd Bldocchi 2003; Misson et l. 2006). In some deciduous tree species, sesonl vrition in photosynthetic response my e linked to sesonl vrition in source ctivity nd sink cpcity (Sholtis et l. 2004). But generlly, rpidly growing deciduous ngiosperms tend to rpidly ccelerte photosynthetic rtes in spring s trees refolite, photosynthesis remins high during summer, nd declines rpidly in utumn s leves senesce efore scising. As result, deciduous trees, which will only hve current-yer leves, must ccomplish ll cron ssimiltion efore the dormnt seson wheres evergreens re cple of continuing to ccumulte dry mtter throughout the yer if environmentl conditions llow. These differences in phenology my explin the significnt differences in photosynthesis over sesons etween these contrsting tree species The role of lef ge in photosynthesis Age-dependent decreses in photosynthesis hve een oserved in rnge of herceous (Hikosk 1996), deciduous (Wilson et l. 2000; Onod et l. 2005) nd evergreen species (Escudero nd Medivill 2003; Miyzw et l. 2004; Niinemets et l. 2005). Such decrese my e explined y: (1) selective degrdtion of ruisco; (2) inctivtion of ruisco; or (3) decresed CO 2 diffusion in old senescing leves s result of incresed mesophyll resistnce (Hikosk nd Tershim 1995; Hikosk et l. 2007). Another explntion for decresing photosynthetic cpcity in older leves is tht the frction of nitrogen llocted to ruisco decreses with incresing lef ge (Wilson et l. 2000; Wilson et l. 2001). This finding is further supported y Rey nd Jrvis (1998) who oserved in their work with irch trees tht the frctionl lloction of nitrogen to ruisco 9

23 Chpter 1 decresed with lef ge, nd this decrese correlted with down-regultion in photosynthesis. Severl other studies hve lso shown tht the reltionship etween nitrogen nd photosynthetic cpcity vries with lef ge. Lef ge driven chnges in photosynthetic cpcity ws lso oserved y Wilson et l. (2000), where rpid increses in V cmx were seen in spring nd decreses in utumn. Similr trends were lso oserved in mple nd ok trees in deciduous forests in Wisconsin (Reich et l. 1991), spen nd red ok trees in Michign (Jurik 1986) nd irch trees in Msschusetts (Bssow nd Bzzz 1998) where lrge reductions in V cmx were evident longside visile evidence of senescence Photosynthetic cclimtion The photosynthetic mchinery in plnts is suject to rnge of environmentl perturtions, nd photosynthetic cclimtion cn occur in response to chnging irrdince, wter or nutrient supply (Turnull et l. 1993; Frk et l. 2001; Noguchi et l. 2001; Kruse et l. 2004). However, since the focus of this thesis is on the effects of temperture chnge on cclimtion, this review will ttempt to provide n in-depth ssessment into the current literture ville on this suject re. Medium nd longterm exposure (one to severl dys, up to full seson) to new temperture regime results in djustments in photosynthesis, cusing the seline responses to shift (Lrcher 1969; Teskey nd Will 1999; Gunderson et l. 2000; Mkel et l. 2004). For instnce, Dougls-fir seedlings were found to hve djusted their photosynthetic response to new therml regime within 10-dy period (Sorensen nd Ferrell 1972). Numerous recent studies hve lso shown tht photosynthesis cn cclimte to chnges in growth 10

24 Chpter 1 temperture, with the result tht rtes of photosynthesis re similr in plnts grown under contrsting therml regimes (complete cclimtion) (Berry nd Bjorkmn 1980; Hurry et l. 1995; Bunce 2000). Complete cclimtion of photosynthesis ws lso oserved some 40 yers go y Mooney nd West (1964) who worked on the dessert shru, Lrre divrict, which ws grown t three dy/night temperture regimes rnging from 20/15 o C to 45/33 o C. All plnts expressed similr photosynthetic rtes when mesured t the corresponding growth tempertures. Furthermore, Turnull et l. (2002) in their work with Populus deltoides exposed to dy time wrming lso concluded tht the optimum temperture of photosynthesis cclimted fully to 6 o C rnge of temperture. However, it hs een oserved tht different species hve vrying potentil for photosynthetic cclimtion (Gunderson et l. 2000; Weston nd Buerle 2007) where some species only disply prtil cclimtion of photosynthesis whilst others exhiit complete cclimtion (Berry nd Bjorkmn 1980; Rogers et l. 1998; Usmi et l. 2001; Sholtis et l. 2004). This vriility in cclimtion is supported y reports from numer of tree species tht hve shown vrying degrees of photosynthetic cclimtion to temperture (Rook 1969; Smith nd Hdley 1974; Strin et l. 1976; Sltyer 1977; Bttgli et l. 1996; Teskey nd Will 1999; Medlyn et l. 2002; Onod et l. 2005; Misson et l. 2006). Much effort hs een plced on gining etter understnding on the mechnisms underpinning the process of photosynthetic cclimtion to higher s well s lower tempertures. For exmple, Berry nd Bjorkmn (1980), Stitt nd Hurry (2002) nd Ymori et l. (2005) hve concluded tht when first exposed to low tempertures, photosynthetic rtes re typiclly strongly reduced. However, with susequent 11

25 Chpter 1 cclimtion, increses in rtes of photosynthesis occur s result of higher degree of unsturtion of memrne lipids nd greter concentrtion of proteins regulting photosynthetic cpcity. But, prolonged exposure to low tempertures cn result in photosynthetic photoinhiition (Lundmrk et l. 1988; Alscher nd Cumming 1990). The susceptiility to photoinhiition results from low tempertures cusing (1) inhiition of photosynthesis therey creting conditions for excessive excittion to occur, (2) inhiition of de novo protein synthesis necessry for repir of photodmge, nd (3) inhiition of lterntive wys of dissipting excessive excittion thus resulting in the ccumultion of potentilly hrmful oxygen species (Schulze nd Cldwell 1994; Morison nd Morecroft 2006). However, plnts often recover fully from cold-induced photoinhiition within hours to dys, depending on species nd the extent of inhiition (Lundmrk et l. 1988). Though the underlying mechnisms involved in photosynthetic cclimtion to chnging environmentl conditions ply key role in our understnding, the iochemicl nd moleculr spects of cclimtion of photosynthesis to chnging tempertures re out of the scope of this thesis, lthough they re currently under intense scrutiny elsewhere (see Sge nd Kuien (2007)) Lef ge nd its effects on photosynthetic cclimtion The developmentl stte of leves nd its role in photosynthetic cclimtion to temperture ws investigted y Yelle et l. (1989), where young leves pprently showed less cclimtion to temperture thn older leves. Mny studies hve lso oserved photosynthetic cclimtion to temperture to e greter in older folige or occurring erlier in older nd lter in younger leves (Turnull et l. 1998; Griffin et l. 12

26 Chpter ; Jch nd Ceulemns 2000; Tissue et l. 2001; Luoml et l. 2003; Mkel et l. 2004). However, other studies hve found tht photosynthetic cclimtion to temperture my e greter in young leves (Vu et l. 1997). This ltter finding is further supported y Strnd et l. (1999) who worked on Aridopsis nd found tht new, young leves developed t the new temperture cclimte more fully to chnges in temperture thn previously developed (older) leves. There is considerle evidence in the literture suggesting tht, lthough cclimtion of photosynthesis to new growth temperture cn occur in pre-existing (older) leves formed t the previous growth temperture, full cclimtion to new growth temperture requires leves to e formed t the new growth temperture ( Hurry et l. 1995; Strnd et l. 1997; Loveys et l. 2002; Atkin et l. 2006). Clerly it is importnt to distinguish etween the direct impcts of lef developmentl ge versus the response of pre-existing nd new leves following temperture chnges Respirtion The primry function of photosynthesis is to ssimilte CO 2 into crohydrtes. A significnt portion of the crohydrte pool then ecomes the min sustrtes of respirtion. The function of respirtion is to convert photossimiltes into products used in growth, mintennce, trnsport nd nutrient ssimiltion processes. The energy conserved during photosynthesis is relesed in iochemiclly regulted mnner for the production of ATP vi respirtion. At the most fundmentl level, respirtion cn e considered to hve dul nture: it is the source of metolic intermedites (cron 13

27 Chpter 1 skeletons) used in the synthesis of cellulr constituents s well s the source of ATP nd reduced nucleotides. Temperture is one of the most importnt environmentl fctors determining the rte of respirtion. However, there is strong evidence suggesting tht the short nd long term response of respirtion to temperture chnge is very different. The Q 10 (the proportionl increse in respirtion for every 10 o C rise in temperture) of respirtion descries the short-term sensitivity of respirtion to temperture. There is, however, no consensus in the literture over the vriility of this temperture coefficient. In recent review, Atkin et l. (2005) concluded tht growth temperture hd no consistent effect on Q 10 vlues. This ws supported y erlier work y Tjoelker et l. (1999) who reported tht the growing temperture environment hd no significnt effect on the Q 10 of respirtion. This hs een further supported y numerous recent reports (Loveys et l. 2003; Armstrong et l. 2006; Atkin et l. 2007; Atkinson et l. 2007) on wide rnge of plnt species. However, some studies hve reported chnging Q 10 (e.g. vlues of Q 10 decrese with incresing temperture) (Sltor 1906; Fuki nd Silsury 1977; Lwrence nd Oechel 1983; Frrr nd Willims 1991; Tjoelker et l. 2001; Zisk et l. 2004). Despite the lck of consensus on the vriility of Q 10, chnges in respirtion rtes with chnging environmentl conditions re widely ccepted finding. Erly reviews focusing on the effects of low temperture on plnt respirtion include those y Lyons nd Rison (1970), Lyons (1973) nd Long nd Woodwrd (1988) these concluded tht respirtory cpcity incresed t low tempertures. This finding ws further supported y work 14

28 Chpter 1 conducted y Frrr nd Willims (1991), Ryn (1995) nd Reich et l. (1996). Similrly, some recent studies hve lso shown tht plnts grown or originting from cold climtes tend to exhiit higher rtes of drk respirtion (Covey-Crump 2002; Lee et l. 2005). By contrst, Egles (1967), Lmers (1985), Criddle et l. (1994) nd Breymeyer et l. (1996) hve reported tht the effects of elevted temperture on respirtion my sometimes vry ut increses in respirtion often correlte positively with incresing tempertures. Becuse this is likely to hve significnt impct on glol cron udgets, mny studies hve since looked t the role of incresing tmospheric tempertures on respirtion s glol records revel wrming trend. Recent reports y Teskey nd Will (1999), Atkin nd Tjoelker (2003), King et l. (2006), Rchmilevitch et l. (2006) nd Wright et l. (2006) hve further confirmed the finding tht respirtion generlly increses with incresing temperture over short time period. In the short-term, chnge in temperture will result in n immedite ltertion in the rte of respirtion, with the extent of tht ltertion determined y the respirtory Q 10. However, long-term exposure to chnge in temperture is likely to result in regultory chnges in respirtory metolism which ring out either prtil or full cclimtion of respirtion (Atkin et l. 2000; Covey-Crump 2002; Griffin et l. 2002; Bolstd et l. 2003; Atkin et l. 2005; Atkin et l. 2006; Armstrong et l. 2006; Morison nd Morecroft 2006; Wright et l. 2006) Respirtory cclimtion Evidence of respirtory cclimtion is extensive, ut the effect vries from no cclimtion (i.e. the instntneous nd the long-term temperture responses re identicl) to complete 15

29 Chpter 1 cclimtion, where rtes mesured t the respective growth tempertures do not differ (Lriguderie nd Korner 1995; Teskey nd Will 1999; Tjoelker et l. 1999; Atkin et l. 2000; Gunderson et l. 2000; Atkin nd Tjoelker 2003; Lee et l. 2005; Turnull et l. 2005). Some preliminry evidence of respirtory cclimtion ws reported some 70 yers go, where the Germn ecophysiologist (Otto Stocker) noted tht leves of tropicl trees in Jv respired t out the sme rte s leves of willows in Greenlnd, when oth were mesured t tempertures in their nturl hitts (reported y Hopkins 1998; Morison nd Morecroft 2006). A more recent exmple is seen in whet cultivrs (Kurimoto et l. 2004; Kurimoto et l. 2004) which were found to exhiit lmost complete cclimtion so tht their rte of respirtion styed constnt over 10 o C shift in growth temperture. Importntly, cclimtion of respirtion to temperture chnge cn e significnt nd rpid (occurring in s quickly s 1-3 dys fter exposure to chnged temperture regimes). Experiments on Quercus species conducted lrgely in the lortory (Bolstd et l. 2003) hve oserved respirtory cclimtion to temperture within two dys. This finding is further supported y Rook (1969), Lriguderie nd Korner (1995), Atkin et l. (2000) nd Ymori et l. (2005). Furthermore, Atkin et l. (2000) nd Gunderson et l. (2000) lso oserved significnt therml cclimtion in field-grown mple seedlings such tht wrm-cclimted seedlings decresed respirtion y 10% compred with cool-cclimted seedlings. In ddition, Tjoelker et l. (1999), in their work with five orel tree species, lso oserved therml cclimtion of respirtion, with cclimtion greter in conifers thn in rodleved species. 16

30 Chpter Mechnisms of cclimtion In recent review on the effects of temperture on respirtion, Atkin et l. (2005) proposed tht there were t lest two different modes of respirtory cclimtion to temperture. Type I cclimtion tht is ssocited with chnge in the rte of respirtion primrily t moderte to higher tempertures, with little to no chnge in respirtion occurring t low mesuring tempertures (i.e. the Q 10 vlue chnges). Type I cclimtion ppers to reflect chnge in the vilility of respirtory sustrtes nd/or the degree of denylte restriction (Atkin nd Tjoelker 2003). Moreover, Type I cclimtion hs een suggested to e rpid, occurring within 1 to 2 dys following chnge in mient temperture (Rook 1969; Atkin et l. 2000; Covey-Crump 2002; Bolstd et l. 2003). Type II cclimtion is ssocited with n increse in the rte of respirtion cross wide rnge of mesurement tempertures (no chnge in the Q 10 of respirtion is necessry in Type II cclimtion). Type II cclimtion is likely to e ssocited with temperture-medited chnges in respirtory cpcity tht cn only e mximlly relised through the formtion of new tissues with ltered folir morphology nd iochemistry (Atkin nd Tjoelker 2003). Type II cclimtion hs een reported to e ssocited with chnges in the reltive mounts of enzymes (e.g. lterntive oxidse (AOX)) The role of lef ge in respirtion As with photosynthesis, the rte of respirtion is lso dependent upon the developmentl stte of tissues, with expnding immture tissues hving higher rtes of respirtion thn fully expnded, mture tissues (Azcon-Bieto nd Osmond 1983; McDonnell nd Frrr 17

31 Chpter ; Atkin nd Cummins 1994; Millr et l. 1998; Armstrong et l. 2006; Atkin et l. 2007). This decrese in respirtion ssocited with tissue expnsion reflects decrese in demnd for ATP required for growth. However, vrious other fctors my lso e responsile for the decrese in rtes of respirtion s tissues expnd these include chnges in protein undnce nd ltertions in the density of mitochondri. Aprt from chnges in respirtion rtes, the developmentl stte of folige hs lso een shown to determine the extent of respirtory cclimtion to temperture in different tissue types (e.g. pre-existing versus new leves). For exmple, newly emerged, young leves (formed t the new temperture environment) hve een shown to e le to exhiit complete cclimtion to chnging environmentl conditions (Loveys et l. 2003; Tlts et l. 2004; Armstrong et l. 2006; Atkin et l. 2006; Atkin et l. 2006). Complete cclimtion in these tissues re possile ecuse new tissues hve the ility to lter their structure (i.e. ntomy/morphology), chemicl composition, nd enzymtic cpcity to the degree required for complete cclimtion of respirtion. However, this finding is y no mens universl nd is likely to e especilly vrile in species with long-lived folige, where complete cclimtion cn occur in pre-existing, mture leves if the tissues re sufficiently long-lived. In short-lived species, such chnges cnnot occur due to senescence of mture leves (Bruhn et l. 2007; Zrgoz-Cstells et l. 2007) Emerging role of the lterntive oxidse (AOX) pthwy in respirtion Higher plnt mitochondri hve two respirtory electron trnsport pthwys. One is the cytochrome (COX) pthwy, which is similr to tht in nimls (hence much is known out it), nd the other is the lterntive-cynide-resistnt pthwy (AOX). Both 18

32 Chpter 1 pthwys re involved in the consumption of sustrte nd in CO 2 emission nd O 2 uptke, ut the lterntive pthwy is nonphosphorylting nd therefore lrgely uncoupled from energy production (lcking in proton trnsloction). The sis of this pthwy is short rnch in the mitochondril electron trnsport chin prior to the cytochrome c oxidse (Lmers 1985). The lterntive pthwy tkes electrons from the uiquinone pool nd psses the electrons to O 2 through n oxidse (AOX) (Amthor 2000). Compred to the cytochrome pthwy, conservtion of energy for the production of ATP is sustntilly reduced, nd free energy initilly generted is lost s het. For most plnts, the precise role of this pthwy hs not een defined, except tht the het produced hs een found to e used y some species (e.g. the spdix of the rum lilies) to voltilise ttrctnts for insect pollintion (Breymeyer et l. 1996). High levels of crohydrtes hve een found to ctivte the AOX pthwy ( Steingrover 1981; Azcon- Bieto nd Osmond 1983). The ltter finding hs led to the suggestion tht AOX my e responsile for consuming excess levels of crohydrtes within plnt vi rpid glycolysis or greter ctivity of the Kres cycle (Lmers 1982). There is emerging evidence in the literture suggesting tht t low tempertures or in cold climtes, higher proportion of mitochondril electron trnsport occurs vi the lterntive (AOX) pthwy (Lmers 1985; Stewrt et l. 1990; Vnlererghe nd McIntosh 1992; Gonzlez-Meler et l. 1999; Kurimoto et l. 2004). For exmple, in the erly 1980s, Kiener nd Brmige (1981) oserved tht chilling hypocotyls of cucumers resulted in n increse in respirtion rte which ws prtly due to incresed ctivity of AOX. This finding ws further supported y Gonzlez-Meler et l. (1999) nd Purvis nd 19

33 Chpter 1 Shewfelt (1993) who lso oserved incresed electron prtitioning to AOX t lower tempertures. Moreover, severl reports (Vnlererghe nd McIntosh 1992; Gonzlez- Meler et l. 1999; Ris-Cro et l. 2000; Atkin et l. 2002; Kurimoto et l. 2004; Fiorni et l. 2005; Atkin et l. 2007) hve lso oserved the sence of AOX ctivity t higher tempertures ut enggement of the AOX pthwy under cooler conditions. Overll, these findings suggest tht AOX my e temperture sensitive nd t low tempertures hs mjor role in plnt respirtion. The significnce of this my e to prevent the formtion of toxic oxygen species tht my result from n over-reduction of the uiquinone pool following inhiition of COX t low tempertures (Purvis nd Shewfelt 1993; Wgner nd Kr 1995; Mxwell et l. 1999; Wright et l. 2006). Additionlly, reports investigting the responses of Q 10 in these two pthwys cme to the conclusion tht the Q 10 of AOX ws lower thn tht of COX (McNulty nd Cummins 1987; Stewrt et l. 1990). However, Gonzlez-Meler et l. (1999) found tht the Q 10 of the AOX nd COX pthwys in mung en leves nd soyen hypocotyls were similr. These conflicting findings in the literture re good resons to suggest tht more reserch is required efore we cn gin n in-depth understnding of the role AOX plys in plnt respirtion. The clssicl pproch used to mesure the ctivity of the AOX nd COX pthwys in isolted s well s in intct tissues involves the use of inhiitors (e.g. potssium cynide (KCN) nd slicylhydroxmic cid (SHAM)). AOX ctivity is determined from the rte of respirtion in the presence of KCN, which locks the COX pthwy, nd corrected for residul respirtion in the presence of oth KCN nd SHAM. COX ctivity is determined 20

34 Chpter 1 from the decrese in the rte of respirtion when SHAM is dded in the sence of KCN. (Hoefngel et l. 1995; Ris-Cro et l. 1995; Noguchi et l. 2001). However, this technique only provide estimtes of mximum rtes of in vivo AOX nd COX ctivity which does not necessrily reflect true in vivo cpcity of oth pthwys. Furthermore, incresed cpcity of either pthwy does not necessrily indicte n increse in the ctul electron flow through oth pthwys in the sence of inhiitors (Dy et l. 1996; Lennon et l. 1997). The only relile methodology presently ville to study electron prtitioning etween AOX nd COX in the sence of inhiitors is the use of the oxygenisotope frctiontion (differences in the isotopic frctiontion of 18 O etween the two terminl oxidses) method (Gonzlez-Meler et l. 1999; Ngel et l. 2001; Noguchi et l. 2001). This technique cn e used on intct tissues or isolted mitochondri nd enzymes (Ris-Cro et l. 2000) Respirtion / photosynthetic (R/P) rtio From the point of view of plnt cron lnce, studying photosynthesis or respirtion in isoltion is prolemtic. Interctions etween these plnt processes must e tken into ccount. Plnt growth should e proportionl to the lnce etween cron gins nd cron losses. Hence, it is importnt to identify the mjor components of this lnce, since it is only when ll the gins nd losses of cron y plnt re considered tht full ccount of the cron lnce, nd growth, cn e mde. Becuse photosynthesis nd respirtion re temperture sensitive, chnge in temperture results in immedite ltertion in the rte of photosynthesis nd respirtion, 21

35 Chpter 1 with the extent eing determined y the temperture coefficient of ech process (Atkin et l. 2007). Mny uthors hve reported tht drk lef respirtion nd photosynthesis re interdependent, with respirtion relying on photosynthesis for sustrte, whilst photosynthesis depends on respirtion for rnge of compounds, such s cron skeletons for protein synthesis nd ATP for sucrose synthesis (Rghvendr et l. 1994; Hoefngel et l. 1995; Hopkins 1998; Thornley nd Cnnell 2000; Atkin et l. 2005; DeLuci et l. 2007). Furthermore, the temperture sensitivity of photosynthesis differs from tht of respirtion nd s result, R/P is ltered following short-term (i.e. minutes to hours) chnges in mesuring temperture (Atkin et l. 2006). However, in mny species, homeostsis of R/P is re-estlished for plnts experiencing contrsting tempertures over sustined periods (i.e. s result of therml cclimtion of specific rtes of respirtion nd photosynthesis) (Dewr et l. 1999; Tjoelker et l. 1999; Gifford 2003; Loveys et l. 2003), lthough this is not universl finding nd it is likely to vry etween species. Nonetheless, lrge mount of support for homeosttic R/P rtio is ville in the literture. For exmple, Gifford (1995) found tht when diverse rnge of species ws grown t constnt tempertures rnging etween 15 to 30 o C, the R/P rtio ws constnt. Likewise, soyen (Glycine mx) grown t rnge of growth tempertures etween 20 nd 35 o C showed no difference in their R/P vlues, owing to cclimtion of respirtion to temperture (Zisk nd Bunce 1997). This conclusion is further supported y Loveys et l. (2002), who lso oserved no difference in R/P vlues of plnts grown t 18 nd 23 o C, ut four out of the six species they investigted exhiited higher R/P vlues t 28 o C. They concluded tht the response of R/P to growth temperture vries with species. Therefore, the generl conclusion is tht R/P is reltively homeosttic t 22

36 Chpter 1 moderte growth tempertures (Gifford 1995; Dewr et l. 1999; Loveys et l. 2003; Atkin et l. 2006; Atkin et l. 2007) ut increses often occur when plnts re exposed to unfvourly high tempertures. Conversely, the sence of homeosttic R/P rtio is lso likely to occur when plnts re exposed to very low tempertures, ecuse respirtion nd photosynthesis do not hve identicl temperture responses to cooler conditions (Atkin et l. 2005; Atkin et l. 2006). Furthermore, respirtion nd photosynthesis my differ in their ility to cclimte to low tempertures (Atkin et l. 2006). In ddition, mny recent reports hve suggested tht, ecuse respirtion is more temperture sensitive in the short-term thn photosynthesis, the R/P rtio is likely to increse under growth conditions of elevted tempertures (Tjoelker et l. 1999; Atkin et l., 2000; Loveys et l. 2002; Atkin et l. 2006; Rchmilevitch et l. 2006; Atkin et l. 2007). Nonetheless, the evidence from numerous studies support the presence of constnt R/P rtio over contrsting growth tempertures, nd glol cron cycle models often ssume homeostsis of this rtio Plnt respirtion in wrmer world Wrming could potentilly increse the iologicl relese of cron to the tmosphere vi plnt respirtion, which t the glol scle currently ccounts for t lest 60 gigtons (Gt) of cron relesed into the tmosphere ech yer. This is mssive flux compred with the reltively smll relese of CO 2 from the comustion of fossil fuels (<6 Gt C yer -1 ) (Houghton et l. 2001; Schimel et l. 2001; Gifford 2003). Both short- nd long-term vrition in mient ir temperture could hve profound effects on the cron lnce of forests. Acclimtion of respirtion to elevted tempertures hs cler implictions for 23

37 Chpter 1 predictions nd expecttions of higher plnt respirtion in wrmer world. For exmple, reduced sensitivity of respirtion to temperture increse (s discussed erlier) could reduce the mgnitude of the positive feedck etween climte nd the cron cycle. With strong cclimtion, ctul lef respirtion t higher tempertures predicted for the end of the 21 st century my well e significntly reduced, nd more cron will e stored in forests (King et l. 2006). This would correspond to less cron relesed ck into the tmosphere nd weker mplifiction of dditionl greenhouse-effect wrming The importnce of nitrogen Tissue N concentrtion is n importnt determinnt of the rte of key physiologicl processes in plnts, such s photosynthesis nd respirtion (Lewis et l. 2004; Tkshim et l. 2004). Like photosynthesis nd respirtion, nitrogen content in leves is temperture sensitive (Rchmilevitch et l. 2006). Lef N origintes from the soil, hence the concentrtion nd totl pools of N within the lef is dependent upon the cpcity of the soil to provide N to the roots nd the cpcity of the root to supply the whole plnt with N (Schulze nd Cldwell 1994; Reich et l. 2006). This distriution of nutrients cn often e ffected y environmentl constrints such s temperture, vpour pressure deficit nd irrdince (Foster nd Aer 1997; Wng et l. 2002; Lewis et l. 2004) Nitrogen (N) nd photosynthetic cclimtion There is overwhelming evidence of strong correltion etween the rte of photosynthesis nd folir N concentrtion (Field nd Mooney 1983; Evns 1989; Reich et l. 1991; Sullivn et l. 1996; Wlcroft et l. 1997; Reich et l. 1998; Crswell et l. 24

38 Chpter ; Dreyer et l. 2001; Frk et l. 2001; Turnull et l. 2002; Tkshim et l. 2004; Diz-Espejo et l. 2006; Morison nd Morecroft 2006; Ysumur et l. 2006), lthough some studies show mixed/inconclusive results (Lwlor 1987; Mchler et l. 1988; Cheng nd Fuchigmi 2000; Wilson et l. 2001). The positive correltion etween N nd photosynthesis my e explined y the proportion of photosynthetic N llocted to ruisco (the nitrogen-rich cron-fixing enzyme), chlorophyll nd the electron trnsport in the thylkoid memrnes ll re importnt in determining rtes of photosynthesis nd, susequently, photosynthetic nitrogen use efficiency (PNUE) (Evns 1989; Foster nd Aer 1997; Frk et l. 2001; Adms 2004; Tkshim et l. 2004; Atkinson et l. 2007; Bown et l. 2007). Incresed lef N is required to support incresed rtes of ruisco croxyltion nd RuBP regenertion vi electron trnsport which re ssocited with incresed rtes of photosynthesis (Wullschleger 1993). Though N is usully considered to e the folir nutrient tht most ffects photosynthesis, conifers in prticulr pper to e less responsive to increse N concentrtions thn most other plnt species (Field nd Mooney 1983; Evns 1989; Boyce et l. 2006). Interestingly, the reltionship etween photosynthesis nd N concentrtion is elieved to lso vry with the developmentl stge of leves (Field 1983; Field nd Mooney 1983; Kull et l. 1998; Wilson et l. 2000; Wilson et l. 2001; Dungn 2003). For exmple, Schoettle nd Smith (1999) found reltionship etween photosynthesis nd nitrogen concentrtion in young folige of Pinus contort (lodgepole pine) ut no reltionship ws found with middle-ged or old folige. This lck of reltionship in older folige ws further confirmed y Rey nd Jrvis (1998), who oserved tht the frctionl lloction of N to ruisco in irch trees 25

39 Chpter 1 decresed with lef ge, nd more importntly, this decese correlted with downregultion in photosynthesis. The ssocition etween N nd photosynthetic cclimtion to environmentl conditions hs received some ttention. There is evidence in the literture suggesting tht photosynthetic cclimtion to elevted CO 2 tends to e more pronounced under N limittion (Bzzz 1990; Gunderson et l. 2002). Nutrient limittion hs een suggested s the driving force for cclimtion in generl, since cclimtion tends to increse PNUE (Curtis 1996). However, experimentl evidence supporting this hypothesis hs so fr een inconclusive (Bunce 1992; Schulze nd Cldwell 1994; Gunderson et l. 2002). Additionlly, ttention hs lso een plced on investigtion of the role of folir N in photosynthetic cclimtion to temperture. For exmple, Mrtindle nd Leegood (1997) concluded tht N supply cn ffect the extent of cold cclimtion of the photosynthetic pprtus, phenomenon tht requires dditionl N investment in chloroplstic nd cytosolic proteins (Stitt nd Hurry 2002). By contrst, photosynthetic cclimtion to elevted tempertures hs een explined y the relloction of N wy from the photosynthetic pprtus to other prts of plnt resulting in reduced photosynthetic rtes (Field et l. 1992; Krpp nd Stitt 1995; Sholtis et l. 2004; Dwyer et l. 2007). It is noteworthy however, tht this down regultion of photosynthesis my not e solely ssocited with the trnsport of N wy from the photosynthetic pprtus, ut my e result of dilution effect rought out y strch nd sugr ccumultion in leves. Furthermore, Misson et l. (2006), in their study on forest ecosystems, suggested tht cclimtion of photosynthetic prmeters to sesonl chnges in temperture re 26

40 Chpter 1 controlled y rnge of fctors (e.g. light, soil wter content nd lef developmentl stge). Nonetheless, N content is considered one of the key fctors determining the plnt s ility to cclimte to sesonl or temperture chnges. This finding is further supported y Field nd Mooney (1983), Breymeyer et l. (1996), Dng et l. (1998), Wilson et l. (2000), Xu nd Bldocchi (2003) nd Grssi et l. (2005). Therefore, we cn conclude tht photosynthetic cclimtion to temperture involves djustments of photosynthetic cpcity nd the relloction of N etween photosynthetic components Nitrogen (N) nd respirtory cclimtion Although the impct of N supply on respirtory cclimtion is not well understood, there is priori evidence suggesting tht N vilility could influence respirtory cclimtion. For exmple, liner reltionships etween lef N nd specific rtes of respirtion hve een found in trees, shrus nd herceous species (Ryn 1995; Reich et l. 1996; Reich et l. 1998; Tjoelker et l. 1999; Dreyer et l. 2001; Griffin et l. 2001; Griffin et l. 2002; Loveys et l. 2003; Turnull et l. 2003; Lee et l. 2005; Morison nd Morecroft 2006; Noguchi nd Tershim 2006; Reich et l. 2006; Atkinson et l. 2007). However, there re lso studies which hve filed to find reltionship etween lef N nd respirtion (Pvlik 1983; Byrd et l. 1992; Poorter et l. 1995; Wng et l. 2002). Interestingly, Tjoelker et l. (1999) oserved tht therml cclimtion of respirtion to higher tempertures in five orel tree species ws lrger for conifers thn rod-leved species nd this ws ssocited with pronounced reductions in lef N concentrtions in conifers t higher tempertures. This difference in responses etween species my e ttriuted to differences in lef structure nd chemistry wherey, unlike the rod-leved 27

41 Chpter 1 species, the needle-leved conifers simply hve greter cpcity to ring out reduction in lef N concentrtion in response to higher growth tempertures. Similrly, Bolstd et l. (2003), working on Quercus tree species, lso concluded tht the downwrd cclimtion of respirtion t higher tempertures is likely to e ttriuted to pronounced reductions in lef N concentrtions. On the other hnd, Ryn (1995), Tjoelker et l. (1999) nd Atkin et l. (2006) hve concluded tht growth in the cold often results in the ccumultion of N in the lef nd this hs een found to e positively correlted to lef respirtion. This conclusion is further supported y the work of Korner (1989) nd Atkin et l. (2006). Cold cclimtion of respirtion is dependent on increses in the cpcity for mitochondril respirtion (Armstrong et l. 2006), which in turn must e supported y n increse in N investment in respirtory protein. Hence, limittions in N supply could restrict the extent to which respirtion cclimtes to low growth tempertures. By contrst, recent report y Atkinson et l. (2007), who worked on severl herceous plnt species grown t oth high nd low N vilility (2000 nd 25 µm, respectively) which were trnsferred from wrm to cooler conditions (25 / 20 o C (dy/night) to 15 / 10 o C), showed tht the ccumultion of N in leves is not essentil for cold cclimtion. Despite the conflicting findings present in the literture, there is strong evidence suggesting tht the degree of cold nd wrm cclimtion my e gretest in leves tht re le to exhiit lrge chnges in the vilility of respirtory sustrtes (i.e. solule sugrs) nd/or nitrogen (i.e. protein) concentrtions (Loveys et l. 2003). 28

42 Chpter Modelling of plnt cron fluxes Models re n importnt tool for understnding forest nd ecosystem function s well s predicting responses to glol chnge. Models help summrise the results of mny individul experiments y incorporting hypotheses nd conclusions into quntittive frmework. Models cn provide estimtes s well s e used in the simultion of longterm experiments. More importntly, models help with the prediction of future rtes of photosynthesis nd respirtion t rnge of scles from the lef level to glol cron cycle models (GCMs) (Atkin et l. 2005). At present, most models ssume tht respirtion nd photosynthesis will increse with temperture in fixed response (i.e. oth processes will not cclimte to future chnges in temperture) (Loveys et l. 2003; Armstrong et l. 2006; Atkin et l. 2006). So fr, rnge of model simultions hve given rise to lrge differences etween estimtes of storge nd fluxes under current nd future climtes (Breymeyer et l. 1996; Aer et l. 2001; Jrvis et l. 2004), so uncertinties still exist out the responses of forests nd ecosystems to chnges in ir temperture nd tmospheric CO 2. For exmple, model estimtes differ in (1) the mount of cron sequestered over forest stnd s lifetime; (2) the response of productivity nd cron relese to incresed tmospheric temperture nd CO 2. The differences in estimtes generted from vrious models suggests tht we re currently still unle to provide ccurte predictions on how cron sequestrtion in vrious forest stnds will respond to future climtic conditions nd much work is still required efore this gol cn e chieved. Although our understnding of the ecophysiology of plnt cron exchnge hs come long wy, it is still fr from eing predictive t glol scle. The chllenges of scling- 29

43 Chpter 1 up from plnts to cnopies, lndscpes, nd even the glol level is the driving force ehind mny efforts in modelling nd innovtive pproches to vlidtions of vrious models. Furthermore, only few models until recently hve simulted how photosynthesis nd respirtion rtes might cclimte to incresed temperture s climte wrming occurs (Korner 1995). Acclimtion is process tht could ffect the response of plnt or forest productivity nd more importntly, influence estimtes of cron relese into the tmosphere over long periods (Bergh et l. 1998; Luo et l. 2001; Loveys et l. 2003; Mkel et l. 2004). Even smll frctionl chnges (s result of cclimtion) in respirtion cn hve lrge impcts on clcultions of cron sequestrtion (Turnull et l. 2005). For exmple, some erly s well s recent ( ) cron lnce models often use sttic Q 10, sttic R d prmeter, or oth, to descrie the short-term response of respirtion nd virtully ignore temperture cclimtion ( list of these models cn e found in Wythers et l. (2005)). The estimtes from these models re often n over prediction of respirtion nd n under prediction of productivity which is especilly evident over long periods. To void the ove inconsistencies, Tjoelker et l. (2001) suggested tht models should incorporte respirtory cclimtion nd temperturedriven Q 10. The inclusion of temperture-vrile prmeters is of even greter significnce if models re to e pplied cross lrge sptil extent where rod rnge of climtes is expected. This suggestion is supported y Gifford (1994), Gifford (1995), Arnone nd Korner (1997), Dewr et l. (1999) nd Gifford (2003) who went further to suggest tht cron cycle models using temperture-driven lgorithms my result in homeostsis of whole-plnt respirtion / photosynthesis (R / P ) in cool to moderte temperture environments (i.e. R / P is insensitive to growth temperture). Therefore, the 30

44 Chpter 1 ove findings suggest tht current modelling of climte chnge nd cron exchnge, which generlly ignores therml cclimtion, my e flwed. For exmple, Wythers et l. (2005) oserved differences (reductions) in folir respirtion nd increses in net primry productivity using temperture-driven prmeters in their PnET ecosystem model. By contrst, Lw et l. (2000) used sttic prmeters to drive n ecosystem model nd cme to the conclusion tht cron relese from Pinus ponderos forest ws enhnced t higher tmospheric tempertures nd productivity negtively ffected. Additionlly, Wythers et l. (2005) lso oserved tht predicted folir respirtion using sttic respirtory prmeters incresed y 8% nd 11% under two other climte wrming scenrios (KONZ nd COWET respectively). However, when modified lgorithms were incorported into the ove models, predicted folir respirtion only incresed y 2 nd 1% respectively. Similrly, King et l. (2006) reported tht the incorportion of cclimtion of lef respirtion into glol ecosystem model (GTEC 2.0) resulted in lower predicted rtes of lef respirtion t higher tempertures nd more cron stored in oth plnts nd soils. These re emerging evidence supporting the use of temperturedriven prmeters in models. Simply dhering to the use of sttic prmeters my contriute to incorrect predictions of future conditions. The influence of cclimtion to temperture hs een found (s seen in erlier sections of this review) to e of significnt mgnitude nd there is incresing evidence tht it should e incorported into plnt, forest or ecosystem climte-cron simultions. 31

45 Chpter Rtionle of the present study From the literture review presented ove, it is cler tht cclimtion of photosynthesis nd respirtion to temperture cn occur in plnts ut my differ in the degree nd speed in which the process tkes plce. Of prticulr focus in this present study re the effects of chnging temperture on the potentil nd extent of photosynthetic nd respirtory cclimtion. It is well documented in the literture tht photosynthesis nd respirtion tend to exhiit qusi-exponentil instntneous response to incresing temperture. However, eyond temperture optimum, rtes of oth processes decline. In the cse of respirtion, the temperture optimum is often much higher thn tht of photosynthesis nd is only reched just elow lethl tempertures. This results in rtes of respirtion rising over greter rnge of tempertures thn photosynthesis. This cn potentilly result in increse emissions of CO 2 t higher tmospheric tempertures, ultimtely cting s positive feedck to the greenhouse effect. It is with this in mind tht I investigted the potentil of cclimtion of oth photosynthesis nd respirtion in oth n evergreen nd deciduous tree species to temperture chnge under oth controlled nd field conditions. The well-estlished hypothesis of positive reltionship etween photosynthesis, respirtion nd nitrogen in the literture led to the investigtion of the role of nutrition (focused solely on N) in the process of cclimtion. Furthermore, since respirtion ws the prmeter of key focus here nd ecuse of previous specultion regrding the role of COX nd AOX pthwys in responses to chnging or stressful conditions, I lso studied chnges in the ctivity of COX nd AOX to temperture chnge. More importntly, the 32

46 Chpter 1 dt collected during the course of this reserch were used to develop n existing leflevel model driven y meteorologicl dt to simulte the effects of temperture on rtes of photosynthesis nd respirtion over long periods nd to generte nnul estimtes of oth processes. This is importnt s presently only few studies hve ccounted for cclimtion of oth photosynthesis nd respirtion in their models. 1.4 Simplified schemtic illustrtion Figure 1 descries the overrching design for this reserch. As previously mentioned, cclimtion of photosynthesis nd respirtion cn occur in rnge of plnt species. However, the extent to which cclimtion occurs in different tissue types (e.g. preexisting nd new tissues) hs not een widely studied. Pre-existing nd new leves cn possess significnt differences in ntomy, iochemistry or morphology s result of chnge in the environment nd these differences my determine the extent to which lef cclimtes to temperture chnge. In ddition, the importnce of nutrition (especilly nitrogen) in photosynthesis nd respirtion is well documented in the literture. Therefore, the role of nitrogen in cclimtion to temperture chnge is likely to e importnt. In this study the role of N ws investigted y compring young trees grown with high nd low levels of N vilility. Furthermore, to dte there hve een few field studies undertken over n entire yer with dt for oth photosynthesis nd respirtion (over different sesons). This lck of dt over long periods hs resulted in models typiclly eing driven y single fixed respirtion rte nd then djusted y fixed Q 10 this gives rise to the potentil for erroneous estimtes. Field nlysis conducted for n entire yer provides dt to ensure tht nnul estimtes of photosynthesis nd respirtion 33

47 Chpter 1 in n evergreen nd deciduous species is more roust, especilly s the process of temperture cclimtion is tken into ccount. 34

48 Chpter 1 Controlled conditions (short term responses): Field (long term responses): Temperture chnge Sesonl effects (temperture) N-vilility (low vs high) CO 2 (Photosynthesis) CO 2 (Respirtion) CO 2 (Photosynthesis) Potentil for photosynthesis nd respirtion to cclimte CO 2 (Respirtion) in pre-existing tissues Chnges in respirtory enzymtic ctivity new tissues formed t new temperture Role of folir crohydrtes in cclimtion Role of folir N concentrtion in cclimtion Dt from controlled nd field experiments used to drive lef-level model to forecst nnul respirtory nd photosynthetic responses to temperture chnge with cclimtion of oth photosynthesis nd respirtion tken into ccount Figure 1.1 Simplified schemtic illustrtion of n investigtion into the potentil for photosynthetic nd respirtory cclimtion under field nd controlled environmentl conditions. 35

49 Chpter Botnicl description of study species Pinus rdit Pinus rdit is ntive of Cliforni, USA. This conifer ws introduced into New Zelnd where it hs ecome the sis of the plnttion timer industry. Pinus rdit ws first plnted on Mount Peel sttion, Cnterury in the erly 1850s. Since then it hs een plnted to form extensive forests throughout New Zelnd. Pinus rdit is n evergreen conifer elonging to the fmily Pincee (Slmon 2000). The tree is cylindricl in shpe nd cn grow m in height. The rnches re upwrd-outwrd spreding nd the rk is drk grey-rown nd deeply fissured. The needles commonly occur in clusters of three held together t the se y tiny scles nd persist on the tree for pproximtely three yers. The mle nd femle flowers re seprte ut on the sme tree. The mles form cylindricl ctkins nd the femles form cones. Pollintion occurs from August to Septemer in the Southern Hemisphere. Pinus rdit is now the most importnt plnttion species in the southern hemisphere. Mjor dvntges of this species re tht it is hrdy, fst growing nd cn dpt to rnge of soil types, ltitudes nd climtic conditions. In New Zelnd, Pinus rdit outgrows lrge numer of tree species on nerly every site, from Northlnd to Southlnd. It produces 20 to 25 cuic metres of wood per hectre ech yer nd is redy to hrvest in 25 to 30 yers. 36

50 Chpter 1 Pinus rdit timer is highly verstile. The light coloured, even textured wood is suitle for furniture, joinery, mouldings, construction, pckging, poles, pulp nd pper. It cn lso e sliced or peeled for veneers nd plywoods nd used in res such s ot uilding. Pinus rdit mde up 85.3% of plnting stock sold in 2007 whilst Pseudotsug menziesii (Dougls fir) remins the second most prominent species, mking up 8.1% of the sles in Hence, the economicl vlue of this species hs led to the development of extensive pine forest esttes. Surveys conducted y the Ministry of Agriculture nd Forestry (MAF) estimtes tht 3000 hectres of new pine forests were plnted in 2007 nd pproximtely hectres were replnted on hrvested res. Figure 1.2 Folige of Pinus rdit (left) nd Populus deltoides (right) species used in this reserch Populus deltoides Poplrs re ntive to Europe, Asi, Afric s well s North nd South Americ. The genus Populus elongs to the fmily Sliccee (Slmon 1999). Next to pines, poplrs re 37