Evaluating the response of δ13C in Haloxylon ammodendron, a dominant C4 species in Asian desert ecosystems, to water and nitrogen addition as well as the availability of its δ13C as an indicator of water use efficiency

Abstract. Variations in precipitation and atmospheric N deposition affect water and N availability in desert and thus may have significant effects on desert ecosystems. Haloxylon ammodendron is a dominant plant in Asian desert, and addressing its physiological acclimatization to the changes in precipitation and N deposition can provide insight into how desert plants adapt to extreme environments by physiological adjustment. Carbon isotope ratio (δ13C) in plants has been suggested as a sensitive long-term indicator of physiological acclimatization. Therefore, this study evaluated the effect of precipitation change and increasing atmospheric N deposition on δ13C of H. ammodendron. Furthermore, H. ammodendron is a C4 plant; whether its δ13C can indicate water use efficiency (WUE) has not been addressed. In the present study, we designed a field experiment with a completely randomized factorial combination of N and water and measured δ13C and gas exchange of H. ammodendron. Then we calculated the degree of bundle-sheath leakiness (φ) and WUE of the assimilating branches of H. ammodendron. δ13C and φ remained stable under N and water supply, while N addition, water addition and their interaction affected gas exchange and WUE in H. ammodendron. In addition, δ13C had no correlation with WUE. These results were associated with the irrelevance between δ13C and the ratio of intercellular to ambient CO2 concentration (ci / ca), which might be caused by a special value (0.37) of the degree of bundle-sheath leakiness (φ) or a lower activity of carbonic anhydrase (CA) of H. ammodendron. In conclusion, δ13C of H. ammodendron is not sensitive to global change in precipitation and atmospheric N deposition and cannot be used for indicating its WUE.

[1]  Xiao-Dong Yang,et al.  High Air Humidity Causes Atmospheric Water Absorption via Assimilating Branches in the Deep-Rooted Tree Haloxylon ammodendron in an Arid Desert Region of Northwest China , 2019, Front. Plant Sci..

[2]  Hailong Yu,et al.  Changes in C:N:P stoichiometry modify N and P conservation strategies of a desert steppe species Glycyrrhiza uralensis , 2018, Scientific Reports.

[3]  J. Araus,et al.  Interactive Effects of CO2 Concentration and Water Regime on Stable Isotope Signatures, Nitrogen Assimilation and Growth in Sweet Pepper , 2018, Front. Plant Sci..

[4]  Xuejun Liu,et al.  Impacts of water and nitrogen addition on nitrogen recovery in Haloxylon ammodendron dominated desert ecosystems. , 2017, The Science of the total environment.

[5]  P. Levy,et al.  Bulk deposition of organic and inorganic nitrogen in southwest China from 2008 to 2013. , 2017, Environmental pollution.

[6]  P. Ellsworth,et al.  Relationship of leaf oxygen and carbon isotopic composition with transpiration efficiency in the C4 grasses Setaria viridis and Setaria italica , 2017, Journal of experimental botany.

[7]  Determination of leaf carbon isotope discrimination in C4 plants under variable N and water supply , 2017, Scientific Reports.

[8]  Fuxi Shi,et al.  Relationship between the stable carbon isotopic composition of modern plants and surface soils and climate: A global review , 2017 .

[9]  H. Schnyder,et al.  Bundle-sheath leakiness and intrinsic water use efficiency of a perennial C4 grass are increased at high vapour pressure deficit during growth , 2016, Journal of experimental botany.

[10]  Jiazhu Li,et al.  A Negative Relationship between Foliar Carbon Isotope Composition and Mass-Based Nitrogen Concentration on the Eastern Slope of Mount Gongga, China , 2016, PloS one.

[11]  P. Ellsworth,et al.  Carbon isotopes and water use efficiency in C4 plants. , 2016, Current opinion in plant biology.

[12]  Jianping Huang,et al.  Accelerated dryland expansion under climate change , 2016 .

[13]  B. Schubert,et al.  Temperature‐induced water stress in high‐latitude forests in response to natural and anthropogenic warming , 2016, Global change biology.

[14]  Wei Sun,et al.  Influence of light and nitrogen on the photosynthetic efficiency in the C4 plant Miscanthus × giganteus , 2016, Photosynthesis Research.

[15]  Meghan L. Avolio,et al.  Characterizing differences in precipitation regimes of extreme wet and dry years: implications for climate change experiments , 2015, Global change biology.

[16]  Markus Reichstein,et al.  Effects of climate extremes on the terrestrial carbon cycle: concepts, processes and potential future impacts , 2015, Global change biology.

[17]  L. Gu,et al.  Nitrogen control of 13 C enrichment in heterotrophic organs relative to leaves in a landscape-building desert plant species , 2014 .

[18]  A. Cousins,et al.  Carbon isotope discrimination as a tool to explore C4 photosynthesis. , 2014, Journal of experimental botany.

[19]  H. Griffiths,et al.  Acclimation to low light by C4 maize: implications for bundle sheath leakiness. , 2014, Plant, cell & environment.

[20]  Dai Yue,et al.  Dynamics of water usage in Haloxylon ammodendron in the southern edge of the Gurbantünggüt Desert , 2014 .

[21]  Klaus Winter,et al.  Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. , 2013, The New phytologist.

[22]  Chris-Carolin Schön,et al.  Stable Carbon Isotope Discrimination Is under Genetic Control in the C4 Species Maize with Several Genomic Regions Influencing Trait Expression1[W] , 2013, Plant Physiology.

[23]  Quan Wang,et al.  Variation of photosynthesis and pigment concentration relative to irradiance and nitrogen content for two coexisting desert shrubs , 2013 .

[24]  Yan Li,et al.  Combined effects of snow depth and nitrogen addition on ephemeral growth at the southern edge of the Gurbantunggut Desert, China , 2013, Journal of Arid Land.

[25]  Keith Goulding,et al.  Enhanced nitrogen deposition over China , 2013, Nature.

[26]  Wei Sun,et al.  The efficiency of C4 photosynthesis under low light conditions in Zea mays, Miscanthus x giganteus and Flaveria bidentis. , 2013, Plant, cell & environment.

[27]  R. Norby,et al.  Elevated CO₂ increases tree-level intrinsic water use efficiency: insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites. , 2013, The New phytologist.

[28]  Fahu Chen,et al.  Variation in the Stable Carbon and Nitrogen Isotope Composition of Plants and Soil along a Precipitation Gradient in Northern China , 2012, PloS one.

[29]  Xiahong Feng,et al.  Response of plants' water use efficiency to increasing atmospheric CO2 concentration. , 2012, Environmental science & technology.

[30]  F. Yao,et al.  Assessment of effects of the rising atmospheric nitrogen deposition on nitrogen uptake and long-term water-use efficiency of plants using nitrogen and carbon stable isotopes. , 2011, Rapid communications in mass spectrometry : RCM.

[31]  N. Grimm,et al.  Ecosystem response to nutrient enrichment across an urban airshed in the Sonoran Desert. , 2011, Ecological applications : a publication of the Ecological Society of America.

[32]  H. Griffiths,et al.  Can the progressive increase of C₄ bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration? , 2010, Plant, cell & environment.

[33]  M. Kohn.  Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate , 2010, Proceedings of the National Academy of Sciences.

[34]  R. Furbank,et al.  Growth of the C4 dicot Flaveria bidentis: photosynthetic acclimation to low light through shifts in leaf anatomy and biochemistry , 2010, Journal of experimental botany.

[35]  K. Mueller,et al.  Global patterns in leaf 13C discrimination and implications for studies of past and future climate , 2010, Proceedings of the National Academy of Sciences.

[36]  Ge Gao,et al.  Simulation of regional temperature and precipitation in the past 50 years and the next 30 years over China , 2010 .

[37]  W. Tan,et al.  Paleovegetation reconstruction using δ 13 C of Soil Organic Matter , 2008 .

[38]  J. Galloway,et al.  Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions , 2008, Science.

[39]  Benjamin L Turner,et al.  Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. , 2007, Journal of experimental botany.

[40]  T. Downing,et al.  Global Desertification: Building a Science for Dryland Development , 2007, Science.

[41]  Youchao Chen,et al.  Microbiotic crusts and their interrelations with environmental factors in the Gurbantonggut desert, western China , 2007 .

[42]  Z. Gu,et al.  The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China , 2007 .

[43]  M. Badger,et al.  Carbonic Anhydrase and Its Influence on Carbon Isotope Discrimination during C4 Photosynthesis. Insights from Antisense RNA in Flaveria bidentis1 , 2006, Plant Physiology.

[44]  Zhou Liping,et al.  Carbon isotope ratios of C 4 plants in loess areas of North China , 2006 .

[45]  Liping Zhou,et al.  Carbon isotope ratios of C4 plants in loess areas of North China , 2006 .

[46]  Liping Zhou,et al.  Carbon isotope ratios of plants and occurrences of C4 species under different soil moisture regimes in arid region of Northwest China , 2005 .

[47]  K. Ma,et al.  Genetic variation within and among populations of a dominant desert tree Haloxylon ammodendron (Amaranthaceae) in China. , 2005, Annals of botany.

[48]  A. Zhisheng,et al.  δ13C variation of C3 and C4 plants across an Asian monsoon rainfall gradient in arid northwestern China , 2005 .

[49]  G. Asner,et al.  Nitrogen Cycles: Past, Present, and Future , 2004 .

[50]  S. Macko,et al.  Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: patterns and implications , 2004 .

[51]  Sheng Jin-hua.  A Study on the Root System of Haloxylon Aammodendron (C.A.Mey.) Bunge , 2004 .

[52]  T L Thompson,et al.  Carbon isotope discrimination and bundle sheath leakiness in three C(4) subtypes grown under variable nitrogen, water and atmospheric CO(2) supply. , 2002, Journal of experimental botany.

[53]  P. Pinter,et al.  Carbon isotope discrimination by Sorghum bicolor under CO2 enrichment and drought , 2001 .

[54]  D. Yakir,et al.  Influence of Carbonic Anhydrase Activity in Terrestrial Vegetation on the 18O Content of Atmospheric CO2 , 2001, Science.

[55]  D. Yakir,et al.  Naturally low carbonic anhydrase activity in C4 and C3 plants limits discrimination against C18OO during photosynthesis , 2000 .

[56]  Xiahong Feng.  Long-term ci /ca response of trees in western North America to atmospheric CO2 concentration derived from carbon isotope chronologies , 1998, Oecologia.

[57]  Frederick C. Meinzer,et al.  Nitrogen stress reduces the efficiency of the C4CO2 concentrating system, and therefore quantum yield, in Saccharum (sugarcane) species , 1998 .

[58]  N. Breda,et al.  Changes of tree-ring δ13C and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century , 1998 .

[59]  J. Ehleringer,et al.  Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects , 1997, Oecologia.

[60]  J. Ehleringer,et al.  Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants , 1995 .

[61]  Peter D. Erskine,et al.  13C Natural Abundance in Plant Communities Along a Rainfall Gradient: a Biological Integrator of Water Availability , 1995 .

[62]  H. Ziegler,et al.  Influence of Nitrogen Supply and Temperature on Stable Carbon Isotope Ratios in Plants of Different Photosynthetic Pathways (C3, C4, CAM) , 1993 .

[63]  Graham D. Farquhar,et al.  Short-term measurements of carbon isotope discrimination in several C4 species , 1992 .

[64]  M. D. Hatch,et al.  Carbonic Anhydrase Activity in Leaves and Its Role in the First Step of C4 Photosynthesis , 1990 .

[65]  M. D. Hatch,et al.  Carbonic anhydrase activity in leaves and its role in the first step of c(4) photosynthesis. , 1990, Plant physiology.

[66]  G. Farquhar,et al.  Isotopic Composition of Plant Carbon Correlates With Water-Use Efficiency of Wheat Genotypes , 1984 .

[67]  M. O'Leary.  Measurement of the isotope fractionation associated with diffusion of carbon dioxide in aqueous solution , 1984 .

[68]  G. Farquhar,et al.  On the Nature of Carbon Isotope Discrimination in C4 Species , 1983 .

[69]  H. Craig.  Carbon 13 in Plants and the Relationships between Carbon 13 and Carbon 14 Variations in Nature , 1954, The Journal of Geology.

[70]  E. Gabrielsen.  Effects of Different Chlorophyll Concentrations on Photosynthesis in Foliage Leaves , 1948 .