楸树种间和种内杂种生长与光合系统氮素利用及分配的差异分析
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摘要
【目的】采用课题组早期创制的楸树种内杂种和种间杂种为试验材料,比较杂种间多年的生长性状及光合生理生化特性。旨在明晰楸树种间和种内杂种的生长及光合能力差异及其原因,探究杂种叶片氮素利用及分配与光合效率的潜在关系,为楸树栽培及遗传改良提供参考。【方法】试验采用完全随机区组设计,测定种内杂种(楸树×楸树, Cbb)和种间杂种(楸树×滇楸, Cbf)1～5年树高和1～6年胸径及6年生时的叶片氮素含量、叶绿素含量、光响应曲线和CO_2响应曲线。采用非直角双曲线模型拟合光响应曲线,FvCB生化模型(Farquhar、von Caemmerer和Berry提出的生物化学光合模型)拟合CO_2响应曲线,分别计算了表观光合量子效率(AQY)、光补偿点(LCP)等气体交换参数及最大羧化效率(V_(c max))、最大电子传递速率(J_(max))等光合生理生化参数。并计算出光合系统(捕光系统,羧化系统和生物力能学组分)氮素分配比例。【结果】方差分析显示2年生以上的种内杂种Cbb树高和胸径均显著大于种间杂种Cbf。种间与种内杂种间叶绿素总量没有显著差异,但Cbf叶绿素b显著高出Cbb 15.08%,Cbb的叶绿素a/b和类胡萝卜素/叶绿素总量比值均显著大于Cbf。Cbb具有更高的最大净光合速率、气孔导度、最大羧化效率和暗呼吸速率,表明了Cbb具有更强的光合能力。种间与种内杂种间叶片氮素含量没有显著差异,但Cbb光系统氮素分配比例相对较高,同时具有更高的光合氮素利用效率,这可能是其高光合效率的主要因素之一。相关分析表明楸树杂种光合氮素利用效率与氮素在羧化系统及生物力能学组分中的分配比例呈显著正相关;种内杂种Cbb光合氮素利用效率与其胸径具有较好的(R~2=0.531)正向线性关系。【结论】1)楸树种内杂种(楸树×楸树)对本地环境(中原地区)具有更强的适应性,致使其生长势显著优于种间杂种(楸树×滇楸); 2)相对于云贵高原,中原地区更长的日照时间和更高的7月均温可能促使了楸树×楸树形成适应高光合辐射环境的响应机制(高水平Chl a/b和Car/Chl a+b); 3)楸树×楸树光合系统更高的N分配比例及高效的N素利用效率提高了其光合能力; 4)楸树种间杂种中滇楸所传递给子代的遗传物质不具有适应中原地区环境的调控机制,这是楸树×滇楸在生长和光合生理方面均劣于楸树×楸树的主要原因。
【Objective】 This study aims to clarify the differences in growth and photosynthetic capacity of intraspecific and interspecific hybrids of Catalpa, and to explore the potential relationship between growth and photosynthetic capacity which is regulated by nitrogen use and distribution in leaves, and to provide favorable basis for Catalpa cultivation and genetic improvement. 【Method】 The experiment was designed with complete random block design, the height of 1-5 years old trees and DBH of 1-6 years old trees of the Catalpa bungei ×C. bungei and C. bungei × C. fargesii f. duclouxii hybrids, and leaf nitrogen content, chlorophyll content, light response curve and CO_2 response curve of the Catalpa hybrids in 6 years old were measured. The non-orthogonal hyperbolic model was used to fit the light response curve to calculate the gas exchange parameters, such as the apparent quantum yield(AQY) and the light compensation point(LCP). The FvCB biochemical model(The biochemical photosynthetic model proposed by Farquhar, von Caemmerer and Berry) was used to fit to the CO_2 response curve, and the maximum carboxylation efficiency(V_(c max)), maximum electron transfer rate(J_(max)) and other photosynthetic biochemical parameters were estimated via the model. Nitrogen allocation ratio in photosynthetic system, include light-harvesting system, carboxylation system and bio-energy component, were calculated. 【Result】 Analysis of variance showed that tree height and DBH of intraspecific hybrids(C. bungei ×C. bungei) were significantly greater than interspecific hybrids(C. bungei × C. fargesii f. duclouxii) after 2 years. There was no significant difference between the two hybrids in the total amount of chlorophyll. But the content of chlorophyll b of interspecific hybrids was significantly higher(15.08%) than intraspecific hybrids. On the other hand, the chlorophyll a/b and carotenoid/chlorophyll a+b of intraspecific hybrids was significantly higher than interspecific hybrids. The photosynthetic parameters showed that the intraspecific hybrid had a greater maximum net photosynthetic rate, stomatal conductance, maximum carboxylation efficiency and dark respiration rate. It showed that they had stronger photosynthetic capacity. There was no significant difference in leaf nitrogen content between the two hybrid types. However, more nitrogen was invested to photosystem for intraspecific hybrid leading to higher photosynthetic nitrogen utilization efficiency(PNUE). And it may be one of the reasons of high photosynthetic efficiency for intraspecific hybrid. Correlation analysis showed that the PNUE of Catalpa hybrids was significantly positively correlated with the nitrogen allocation in the carboxylation system and bioenergetics. In addition, the PNUE of intraspecific hybrid had a greater(R~2=0.531) positive linear relationship with the diameter at breast height(DBH).【Conclusion】 1) Intraspecific hybrids have a stronger adaptability to the local environment(The central plains), it was the reason that growth of Catalpa bungei×C. bungei was significantly better than interspecific hybrid(C. bungei × C. fargesii f. duclouxii). 2) Compared with Yunnan-Guizhou plateau, the longer sunshine duration and higher mean temperature in July in the central plains may be the reason for the formation of a response mechanism(high level Chl a/b and Car/Chl a+b) for intraspecific hybrid to adapt to the high photosynthetic radiation environment. 3) Higher N distribution ratio and N use efficiency in photosynthetic system of C. bungei×C. bungei improved its photosynthetic ability. 4) The genetic material transmitted to the offspring by C. fargesii f. duclouxii did not have the regulatory mechanism to adapt to the environment in the central plains, this is the main reason why the growth and photosynthetic physiology of interspecific hybrids are inferior to that of intraspecific hybrids in the central plains.
【Objective】 This study aims to clarify the differences in growth and photosynthetic capacity of intraspecific and interspecific hybrids of Catalpa, and to explore the potential relationship between growth and photosynthetic capacity which is regulated by nitrogen use and distribution in leaves, and to provide favorable basis for Catalpa cultivation and genetic improvement. 【Method】 The experiment was designed with complete random block design, the height of 1-5 years old trees and DBH of 1-6 years old trees of the Catalpa bungei ×C. bungei and C. bungei × C. fargesii f. duclouxii hybrids, and leaf nitrogen content, chlorophyll content, light response curve and CO_2 response curve of the Catalpa hybrids in 6 years old were measured. The non-orthogonal hyperbolic model was used to fit the light response curve to calculate the gas exchange parameters, such as the apparent quantum yield(AQY) and the light compensation point(LCP). The FvCB biochemical model(The biochemical photosynthetic model proposed by Farquhar, von Caemmerer and Berry) was used to fit to the CO_2 response curve, and the maximum carboxylation efficiency(V_(c max)), maximum electron transfer rate(J_(max)) and other photosynthetic biochemical parameters were estimated via the model. Nitrogen allocation ratio in photosynthetic system, include light-harvesting system, carboxylation system and bio-energy component, were calculated. 【Result】 Analysis of variance showed that tree height and DBH of intraspecific hybrids(C. bungei ×C. bungei) were significantly greater than interspecific hybrids(C. bungei × C. fargesii f. duclouxii) after 2 years. There was no significant difference between the two hybrids in the total amount of chlorophyll. But the content of chlorophyll b of interspecific hybrids was significantly higher(15.08%) than intraspecific hybrids. On the other hand, the chlorophyll a/b and carotenoid/chlorophyll a+b of intraspecific hybrids was significantly higher than interspecific hybrids. The photosynthetic parameters showed that the intraspecific hybrid had a greater maximum net photosynthetic rate, stomatal conductance, maximum carboxylation efficiency and dark respiration rate. It showed that they had stronger photosynthetic capacity. There was no significant difference in leaf nitrogen content between the two hybrid types. However, more nitrogen was invested to photosystem for intraspecific hybrid leading to higher photosynthetic nitrogen utilization efficiency(PNUE). And it may be one of the reasons of high photosynthetic efficiency for intraspecific hybrid. Correlation analysis showed that the PNUE of Catalpa hybrids was significantly positively correlated with the nitrogen allocation in the carboxylation system and bioenergetics. In addition, the PNUE of intraspecific hybrid had a greater(R~2=0.531) positive linear relationship with the diameter at breast height(DBH).【Conclusion】 1) Intraspecific hybrids have a stronger adaptability to the local environment(The central plains), it was the reason that growth of Catalpa bungei×C. bungei was significantly better than interspecific hybrid(C. bungei × C. fargesii f. duclouxii). 2) Compared with Yunnan-Guizhou plateau, the longer sunshine duration and higher mean temperature in July in the central plains may be the reason for the formation of a response mechanism(high level Chl a/b and Car/Chl a+b) for intraspecific hybrid to adapt to the high photosynthetic radiation environment. 3) Higher N distribution ratio and N use efficiency in photosynthetic system of C. bungei×C. bungei improved its photosynthetic ability. 4) The genetic material transmitted to the offspring by C. fargesii f. duclouxii did not have the regulatory mechanism to adapt to the environment in the central plains, this is the main reason why the growth and photosynthetic physiology of interspecific hybrids are inferior to that of intraspecific hybrids in the central plains.
引文
鲍甫成,罗建举.2002.桉树纸浆材生长、材性指标近交退化和杂种优势分析.北京林业大学学报,24(3):1-6.(Bao F C,Luo J J.2002.Inbreeding depression and hybrid superiority in growth and wood traits of eucalypt pulp wood.Journal of Beijing Forestry University,24(3):1-6.[in Chinese])
樊莉丽,彭方仁,王改萍,等.2013.楸树自交及种内、种间杂交亲和性的细胞学观察.南京林业大学学报:自然科学版,37(4):1-7.(Fan L L,Peng F R,Wang G P,et al.2013.Cytological observation of fertilization compatibility of Catalpa bungei after self,intraspecific cross and interspecific cross-pollination.Journal of Nanjing Forestry University:Natural Sciences,37(4):1-7.[in Chinese])
户田良吉.1992.当代林木育种.陶章安译.北京:中国林业出版社.(Toda R.1992.Modern Advances in Tree Breeding.Translated by Tao Z A.Beijing:China Forestry Publishing House.[in Chinese])
贾继文,王军辉,张金凤,等.2010.楸树与滇楸种间杂交的初步研究.林业科学研究,23(3):382-386.(Jia J W,Wang J H,Zhang J F,et al.2010.Interspecific hybridization of Catalpa bungei and Catalpa fargesii f.duclouxii.Forest Research,23(3):382-386.[in Chinese])
王学奎,黄见良.2015.植物生理生化实验原理与技术.北京:高等教育出版社,131-133.[in Chinese]).(Wang X K,Huang J L.2015.Principles and techniques of plant physiological biochemical experiment.Beijing:Higher Education Press,131-133.[in Chinese])
吴丽华,王军辉,林娟.2010.楸树植物资源的研究概况.上海交通大学学报:农业科学版,28(1):91-96.(Wu L H,Wang J H,Lin J.2010.A survey of the studies on the resources of Catalpa bungei.Journal of Shanghai Jiaotong University:Agricultural Science,28(1):91-96.[in Chinese])
许晨璐,孙晓梅,张守攻.2012.日本落叶松与长白落叶松及其杂种光合特性比较.北京林业大学学报,34(4):62-66.(Xu C L,Sun X M,Zhang S G.2012.Comparison in photosynthetic characteristics of Larix kaempferi,L.olgensis and their hybrids.Journal of Beijing Forestry University,34(4):62-66.[in Chinese])
Abbott R J.1992.Plant invasions,interspecific hybridization and the evolution of new plant taxa.Trends in Ecology & Evolution,7(12):401-405.
Baltzer J L,Thomas S C,Nilus R,et al.2005.Edaphic specialization tropical trees:physiological correlates and responses to reciprocal transplantation.Ecology,86(11):3063-3077.
Berguson W E,Mcmahon B G,Riemenschneider D E.2017.Additive and non-additive genetic variances for tree growth in several hybrid poplar populations and implications regarding breeding strategy.Silvae Genetica,66(1):33-39.
Bradshaw H D,Ceulemans R,Davis J,et al.2000.Emerging model systems in plant biology:Poplar (Populus) as a model forest tree.J Plant Growth Regul,19(3):306-313.
Bungard R A,Ruban A V,Hibberd J M,et al.1999.Unusual carotenoid composition and a new type of xanthophyll cycle in plants.Proceedings of the National Academy of Sciences of the United States of America,96(3):1135-1139.
Dillen S Y,Marron N,Sabatti M,et al.2009.Relationships among productivity determinants in two hybrid poplar families grown during three years at two contrasting sites.Tree Physiology,29(8):975-987.
Erley G S A,Wijaya K A,Ulas A.2007.Leaf senescence and N uptake parameters as selection traits for nitrogen efficiency of oilseed rape cultivars.Physiologia Plantarum,130(4):519-531.
Evans J R,Seemann J R.1989.The allocation of nitrogen in the photosynthetic apparatus:costs,consequences and control.Plant Biology,8:183-205.
Farquhar G D,von Caemmerer S,Berry J A.1980.A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Planta,149:178-190.
Grubb P J.1977.The maintenance of species-richness in plant communities:the importance of the regeneration niche.Biological Reviews,52(1):107-145.
Gu L,Pallardy S G,Tu K,et al.2010.Reliable estimation of biochemical parameters from C-3 leaf photosynthesis-intercellular carbon dioxide response curves.Plant Cell & Environment,33(11):1852-1874.
Guan L L,Wen D Z.2011.More nitrogen partition in structural proteins and decreased photosynthetic nitrogen use efficiency of Pinus massoniana under in situ polluted stress.Journal of Plant Research,124(6):663-673.
Jennings D L,Brydon E.2010.Further studies on resistance to Leptosphaeria coniothyrium in the red raspberry and related species.Annals of Applied Biology,115(3):499-506.
Killingbeck K T,Whitford W G.2001.Nutrient resorption in shrubs growing by design,and by default in Chihuahuan Desert arroyos.Oecologia,128(3):351-359.
LeBauer D S,Treseder K K.2008.Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed.Ecology,89(2):371-379.
Leverenz J W,Jarvis P G.1979.Photosynthesis in Sitka spruce VIII:The effects of light flux density and direction on the rate of net photosynthesis and the stomatal conductance of needles.Journal of Applied Ecology,16(3):919-932.
Lu P,Colombo S J,Sinclair R W.2007.Cold hardiness of interspecific hybrids between Pinus strobus and P.wallichiana measured by post-freezing needle electrolyte leakage.Tree Physiology,27(2):243-250.
Luo G,Xue L,Guo R,et al.2017.Creating cold resistant strawberry via interploidy hybridization between octoploid and dodecaploid.Euphytica,213(8):194.
Madhibha T,Murepa R,Musokonyi C,et al.2013.Genetic parameter estimates for interspecific Eucalyptus hybrids and implications for hybrid breeding strategy.New Forests,44(1):63-84.
Mao Q Z,Watanabe M,Imori M,et al.2012.Photosynthesis and nitrogen allocation in needles in the sun and shade crowns of hybrid larch saplings:effect of nitrogen application.Photosynthetica,50(3):422-428.
Marron N,Ricciotti L,Bastien C,et al.2010.Plasticity of growth and biomass production of an intraspecific Populus alba family grown at three sites across Europe during three growing seasons.Canadian Journal of Forest Research,40(10):1887-1903.
Mathur S,Jain L,Jajoo A.2018.Photosynthetic efficiency in sun and shade plants.Photosynthetica,56(1):354-365.
Niinemets U,Kull O,Tenhunen J D.1998.An analysis of light effects on foliar morphology,physiology,and light interception in temperate deciduous woody species of contrasting shade tolerance.Tree Physiology,18(10):681-696.
Niinemets U,Tenhunen J D.1997.A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum.Plant Cell & Environment,20(7):845-866.
Potts B M,Dungey H S.2004.Interspecific hybridization of Eucalyptus:key issues for breeders and geneticists.New Forests,27(2):115-138.
Reich P B,Walters M B,Tabone T J.1989.Response of Ulmus americana seedlings to varying nitrogen and water status 2:Water and nitrogen use efficiency in photosynthesis.Tree Physiology,5(2):173-184.
Ripullone F,Grassi G,Lauteri M,et al.2003.Photosynthesis-nitrogen relationships:interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment.Tree Physiology,23(2):137-144.
Sharwood R E,Crous K Y,Whitney S M,et al.2017.Linking photosynthesis and leaf N allocation under future elevated CO2 and climate warming in Eucalyptus globulus.Journal of Experimental Botany,68(5):1157-1167.
Takashima T,Hikosaka K,Hirose T.2004.Photosynthesis or persistence:nitrogen allocation in leaves of evergreen and deciduous Quercus species.Plant,Cell & Environment,27(8):1047-1054.
Taylor L R,Whittaker R H,Levin S A.1977.Niche:Theory and application.Journal of Animal Ecology,46(3):978.
Zanewich K P,Pearce D W,Rood S B.2018.Heterosis in poplar involves phenotypic stability:cottonwood hybrids outperform their parental species at suboptimal temperatures.Tree Physiology,36(8):789-800.
樊莉丽,彭方仁,王改萍,等.2013.楸树自交及种内、种间杂交亲和性的细胞学观察.南京林业大学学报:自然科学版,37(4):1-7.(Fan L L,Peng F R,Wang G P,et al.2013.Cytological observation of fertilization compatibility of Catalpa bungei after self,intraspecific cross and interspecific cross-pollination.Journal of Nanjing Forestry University:Natural Sciences,37(4):1-7.[in Chinese])
户田良吉.1992.当代林木育种.陶章安译.北京:中国林业出版社.(Toda R.1992.Modern Advances in Tree Breeding.Translated by Tao Z A.Beijing:China Forestry Publishing House.[in Chinese])
贾继文,王军辉,张金凤,等.2010.楸树与滇楸种间杂交的初步研究.林业科学研究,23(3):382-386.(Jia J W,Wang J H,Zhang J F,et al.2010.Interspecific hybridization of Catalpa bungei and Catalpa fargesii f.duclouxii.Forest Research,23(3):382-386.[in Chinese])
王学奎,黄见良.2015.植物生理生化实验原理与技术.北京:高等教育出版社,131-133.[in Chinese]).(Wang X K,Huang J L.2015.Principles and techniques of plant physiological biochemical experiment.Beijing:Higher Education Press,131-133.[in Chinese])
吴丽华,王军辉,林娟.2010.楸树植物资源的研究概况.上海交通大学学报:农业科学版,28(1):91-96.(Wu L H,Wang J H,Lin J.2010.A survey of the studies on the resources of Catalpa bungei.Journal of Shanghai Jiaotong University:Agricultural Science,28(1):91-96.[in Chinese])
许晨璐,孙晓梅,张守攻.2012.日本落叶松与长白落叶松及其杂种光合特性比较.北京林业大学学报,34(4):62-66.(Xu C L,Sun X M,Zhang S G.2012.Comparison in photosynthetic characteristics of Larix kaempferi,L.olgensis and their hybrids.Journal of Beijing Forestry University,34(4):62-66.[in Chinese])
Abbott R J.1992.Plant invasions,interspecific hybridization and the evolution of new plant taxa.Trends in Ecology & Evolution,7(12):401-405.
Baltzer J L,Thomas S C,Nilus R,et al.2005.Edaphic specialization tropical trees:physiological correlates and responses to reciprocal transplantation.Ecology,86(11):3063-3077.
Berguson W E,Mcmahon B G,Riemenschneider D E.2017.Additive and non-additive genetic variances for tree growth in several hybrid poplar populations and implications regarding breeding strategy.Silvae Genetica,66(1):33-39.
Bradshaw H D,Ceulemans R,Davis J,et al.2000.Emerging model systems in plant biology:Poplar (Populus) as a model forest tree.J Plant Growth Regul,19(3):306-313.
Bungard R A,Ruban A V,Hibberd J M,et al.1999.Unusual carotenoid composition and a new type of xanthophyll cycle in plants.Proceedings of the National Academy of Sciences of the United States of America,96(3):1135-1139.
Dillen S Y,Marron N,Sabatti M,et al.2009.Relationships among productivity determinants in two hybrid poplar families grown during three years at two contrasting sites.Tree Physiology,29(8):975-987.
Erley G S A,Wijaya K A,Ulas A.2007.Leaf senescence and N uptake parameters as selection traits for nitrogen efficiency of oilseed rape cultivars.Physiologia Plantarum,130(4):519-531.
Evans J R,Seemann J R.1989.The allocation of nitrogen in the photosynthetic apparatus:costs,consequences and control.Plant Biology,8:183-205.
Farquhar G D,von Caemmerer S,Berry J A.1980.A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Planta,149:178-190.
Grubb P J.1977.The maintenance of species-richness in plant communities:the importance of the regeneration niche.Biological Reviews,52(1):107-145.
Gu L,Pallardy S G,Tu K,et al.2010.Reliable estimation of biochemical parameters from C-3 leaf photosynthesis-intercellular carbon dioxide response curves.Plant Cell & Environment,33(11):1852-1874.
Guan L L,Wen D Z.2011.More nitrogen partition in structural proteins and decreased photosynthetic nitrogen use efficiency of Pinus massoniana under in situ polluted stress.Journal of Plant Research,124(6):663-673.
Jennings D L,Brydon E.2010.Further studies on resistance to Leptosphaeria coniothyrium in the red raspberry and related species.Annals of Applied Biology,115(3):499-506.
Killingbeck K T,Whitford W G.2001.Nutrient resorption in shrubs growing by design,and by default in Chihuahuan Desert arroyos.Oecologia,128(3):351-359.
LeBauer D S,Treseder K K.2008.Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed.Ecology,89(2):371-379.
Leverenz J W,Jarvis P G.1979.Photosynthesis in Sitka spruce VIII:The effects of light flux density and direction on the rate of net photosynthesis and the stomatal conductance of needles.Journal of Applied Ecology,16(3):919-932.
Lu P,Colombo S J,Sinclair R W.2007.Cold hardiness of interspecific hybrids between Pinus strobus and P.wallichiana measured by post-freezing needle electrolyte leakage.Tree Physiology,27(2):243-250.
Luo G,Xue L,Guo R,et al.2017.Creating cold resistant strawberry via interploidy hybridization between octoploid and dodecaploid.Euphytica,213(8):194.
Madhibha T,Murepa R,Musokonyi C,et al.2013.Genetic parameter estimates for interspecific Eucalyptus hybrids and implications for hybrid breeding strategy.New Forests,44(1):63-84.
Mao Q Z,Watanabe M,Imori M,et al.2012.Photosynthesis and nitrogen allocation in needles in the sun and shade crowns of hybrid larch saplings:effect of nitrogen application.Photosynthetica,50(3):422-428.
Marron N,Ricciotti L,Bastien C,et al.2010.Plasticity of growth and biomass production of an intraspecific Populus alba family grown at three sites across Europe during three growing seasons.Canadian Journal of Forest Research,40(10):1887-1903.
Mathur S,Jain L,Jajoo A.2018.Photosynthetic efficiency in sun and shade plants.Photosynthetica,56(1):354-365.
Niinemets U,Kull O,Tenhunen J D.1998.An analysis of light effects on foliar morphology,physiology,and light interception in temperate deciduous woody species of contrasting shade tolerance.Tree Physiology,18(10):681-696.
Niinemets U,Tenhunen J D.1997.A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum.Plant Cell & Environment,20(7):845-866.
Potts B M,Dungey H S.2004.Interspecific hybridization of Eucalyptus:key issues for breeders and geneticists.New Forests,27(2):115-138.
Reich P B,Walters M B,Tabone T J.1989.Response of Ulmus americana seedlings to varying nitrogen and water status 2:Water and nitrogen use efficiency in photosynthesis.Tree Physiology,5(2):173-184.
Ripullone F,Grassi G,Lauteri M,et al.2003.Photosynthesis-nitrogen relationships:interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment.Tree Physiology,23(2):137-144.
Sharwood R E,Crous K Y,Whitney S M,et al.2017.Linking photosynthesis and leaf N allocation under future elevated CO2 and climate warming in Eucalyptus globulus.Journal of Experimental Botany,68(5):1157-1167.
Takashima T,Hikosaka K,Hirose T.2004.Photosynthesis or persistence:nitrogen allocation in leaves of evergreen and deciduous Quercus species.Plant,Cell & Environment,27(8):1047-1054.
Taylor L R,Whittaker R H,Levin S A.1977.Niche:Theory and application.Journal of Animal Ecology,46(3):978.
Zanewich K P,Pearce D W,Rood S B.2018.Heterosis in poplar involves phenotypic stability:cottonwood hybrids outperform their parental species at suboptimal temperatures.Tree Physiology,36(8):789-800.
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