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Sex-specific physiological and growth responses to elevated temperature and CO2 concentration in Chinese seabuckthorn (Hippophae rhamnoides subsp. sinensis Rousi)

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Abstract

To examine whether females and males of Chinese seabuckthorn (Hippophae rhamnoides subsp. sinensis Rousi) differ in their responses to elevated atmospheric carbon dioxide (CO2) and temperature, we examined gender-specific physiological and growth responses of H. rhamnoides, exposed to elevated temperature (ET), elevated CO2 concentration (EC), and their interaction (ECT) in environmentally controlled growth chambers. We found that ET significantly decreased the high growth rate (HGR) in both sexes. There were gender differences in biomass accumulation, photosynthetic capacity, nutrient absorption, and nonstructural carbohydrate (NSCs) contents under ET condition. The growth of females was more inhibited by ET than did males. EC significantly increased HGR, net photosynthetic rate (Pn), and biomass accumulation in both sexes, especially for males. Moreover, physiological and biochemical parameters, such as root nodule biomass and N content, showed greater gender differences under ECT than under EC and ET conditions. For both females and males, ECT increased HGR, biomass accumulation, Pn, and water use efficiency (WUE). We conclude that H. rhamnoides males and females exhibited sexually differential responses to climate change.

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All data generated or analyzed during this study are included in this published article. The datasets of raw data generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Agathokleous E, Belz RG, Kitao M, Koike T, Calabrese EJ (2018) Does the root to shoot ratio show a hormetic response to stress? An ecological and environmental perspective. J Forestry Res 30:1569–1580

    Article  Google Scholar 

  • Becklin KM, Walker SM, Way DA, Ward JK (2017) CO2 studies remain key to understanding a future world. New Phytol 214:34–40

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Coleman JS, Bazzaz FA, McConnaughay KDM (2000) Biomass allocation in old-field annual species grown in elevated CO2 environments: no evidence for optimal partitioning. Global Change Biol 6:855–863

    Article  Google Scholar 

  • Cai C et al (2016) Responses of wheat and rice to factorial combinations of ambient and elevated CO2 and temperature in FACE experiments. Global Change Biol 22:856–874

    Article  Google Scholar 

  • Chen LH, Dong TF, Duan BL (2014) Sex-specific carbon and nitrogen partitioning under N deposition in Populus cathayana. Trees-Struct Funct 28:793–806

    Article  CAS  Google Scholar 

  • Chen J, Liu Q, Yu L, Korpelainen H, Niinemets Ü, Li C (2021) Elevated temperature and CO2 interactively modulate sexual competition and ecophysiological responses of dioecious Populus cathayana. Forest Ecol Manag 481:118747

    Article  Google Scholar 

  • Chitarra W, Siciliano I, Ferrocino I, Gullino ML, Garibaldi A (2015) Effect of elevated atmospheric CO2 and temperature on the disease severity of rocket plants caused by fusarium wilt under phytotron conditions. PLoS One 10:e0140769

    Article  PubMed  PubMed Central  Google Scholar 

  • Davey P, Ölçer Footitt H, Zakhleniuk O, Bernacchi C, Calfapietra C, Long S, Raines C (2006) Can fast-growing plantation trees escape biochemical down-regulation of photosynthesis when grown throughout their complete production cycle in the open air under elevated carbon dioxide? Plant Cell Environ 29:1235–1244

    Article  CAS  PubMed  Google Scholar 

  • Dawes MA, Schleppi P, Hattenschwiler S, Rixen C, Hagedorn F (2017) Soil warming opens the nitrogen cycle at the alpine treeline. Global Change Biol 23:421–434

    Article  Google Scholar 

  • De la Riva E, Villar R, Poorter H, Olmo M, Ubera J (2016) Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 mediterranean woody species along a water availability gradient. PLoS One 11:e0148788

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng SB, Hu BY, Chen T, Wang B, Huang J, Wang YJ, Yu G (2015) Activated carbons prepared from peanut shell and sunflower seed shell for high CO2 adsorption. Adsorption 21:125–133

    Article  CAS  Google Scholar 

  • Dolkar P, Dolkar D, Kant A, Chaurasia OP, Stobdan T (2017) Gender-specific seasonal pattern and altitudinal variation in freeze tolerance responses of Seabuckthorn (Hippophae rhamnoides L.). J Berry Res 7:291–297

    Article  CAS  Google Scholar 

  • Du Y, Lu RL, Xia JY (2020) Impacts of global environmental change drivers on non-structural carbohydrates in terrestrial plants. Funct Ecol 34:1525–1536

    Article  Google Scholar 

  • Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221:32–49

    Article  CAS  PubMed  Google Scholar 

  • Evans JR, Clarke VC (2019) The nitrogen cost of photosynthesis. J Exp Bot 70:7–15

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Martinez M et al (2019) Global trends in carbon sinks and their relationships with CO2 and temperature. Nat Clim Change 9:73–79

    Article  CAS  Google Scholar 

  • Fischinger SA, Hristozkova M, Mainassara ZA, Schulze J (2010) Elevated CO2 concentration around alfalfa nodules increases N2 fixation. J Exp Bot 61:121–130

    Article  CAS  PubMed  Google Scholar 

  • Hebbar KB, Apshara E, Chandran KP, Prasad PVV (2020) Effect of elevated CO2, high temperature, and water deficit on growth, photosynthesis, and whole plant water use efficiency of cocoa (Theobroma cacao L.). Int J Biometeorol 64:47–57

    Article  CAS  PubMed  Google Scholar 

  • Jones M, Macdonald S, Henry G (1999) Sex- and habitat-specific responses of a high arctic willow, Salix arctica, to experimental climate change. Oikos 87:129–138

    Article  Google Scholar 

  • Keenan TF, Hollinger DY, Bohrer G, Dragoni D, Munger JW, Schmid HP, Richardson AD (2013) Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499:324–327

    Article  CAS  PubMed  Google Scholar 

  • Kumar Y, Sze-Wan P, Gachon C, Brodie J, Sade A, Lim PE (2020) Impact of elevated temperature on the physiological and biochemical responses of Kappaphycus alvarezii (Rhodophyta). PLoS One 15:e0239097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li CY, Xu G, Zang RG, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406

    Article  CAS  PubMed  Google Scholar 

  • Li L, Zhang Y, Luo J, Korpelainen H, Li C (2012) Sex-specific responses of populus yunnanensis exposed to elevated CO2 and salinity. Physiol Plantarum 147:477–488

    Article  Google Scholar 

  • Li P, Li H, Zong Y, Li F, Han Y, Hao X (2017a) Photosynthesis and metabolite responses of Isatis indigotica fortune to elevated [CO2]. The Crop Journal 5:345–353

    Article  Google Scholar 

  • Li YS, Yu ZH, Liu XB, Mathesius U, Tang CX, Wu JJ, Liu JD, Zhang SQ, Jin J (2017b) Elevated CO2 increases nitrogen fixation at the reproductive phase contributing to various yield responses of soybean cultivars. Front Plant Sci 8:1546

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Manning W, Wang X (2019) Elevated CO2 increases root mass and leaf nitrogen resorption in red maple (Acer rubrum L.). Forests 10:420

    Article  Google Scholar 

  • Liao J, Song HF, Tang DT, Zhang S (2019) Sexually differential tolerance to water deficiency of Salix paraplesia-A female-biased alpine willow. Ecol Evol 9:8450–8464

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YY, Wu LH, Baddeley JA, Watson CA (2011) Models of biological nitrogen fixation of legumes: a review. Agron Sustain Dev 31:155–172

    Article  Google Scholar 

  • Liu J, Zhang R, Xu X, Fowler JC, Miller TEX, Dong T (2020a) Effect of summer warming on growth, photosynthesis and water status in female and male Populus cathayana: implications for sex-specific drought and heat tolerances. Tree Physiol 40:1178–1191

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Liu X, Kang J, Korpelainen H, Li C (2020b) Are males and females of Populus cathayana differentially sensitive to Cd stress? J Hazard Mater 393:122411

    Article  CAS  PubMed  Google Scholar 

  • Long S, Ainsworth E, Rogers A, Ort D (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628

    Article  CAS  PubMed  Google Scholar 

  • Ma F, Xu TT, Ji MF, Zhao CM (2015) Responses of two endemic species of Hippophae at the qinghai-tibet plateau to elevated CO2 concentration. Photosynthetica 53:395–402

    Article  CAS  Google Scholar 

  • Martinez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86:495–516

    Article  Google Scholar 

  • Melnikova NV, Borkhert EV, Snezhkina AV, Kudryavtseva AV, Dmitriev AA (2017) Sex-specific response to stress in Populus. Front Plant Sci 8:1827

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell AK (1998) Acclimation of pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757

    Article  PubMed  Google Scholar 

  • Murray TJ, Tissue DT, Ellsworth DS, Riegler M (2013) Interactive effects of pre-industrial, current and future [CO2] and temperature on an insect herbivore of Eucalyptus. Oecologia 171:1025–1035

    Article  CAS  PubMed  Google Scholar 

  • Nelson DW, Sommers L, Page AL, Miller RH, Keeney DR (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2: chemical and microbiological properties. The American Society of Agronomy, Madison, pp 539–552

    Google Scholar 

  • Nissinen K, Nybakken L, Virjamo V, Julkunen-Tiitto R (2016) Slow-growing Salix repens (Salicaceae) benefits from changing climate. Environ Exp Bot 128:59–68

    Article  Google Scholar 

  • Noyce GL, Kirwan ML, Rich RL, Megonigal JP (2019) Asynchronous nitrogen supply and demand produce nonlinear plant allocation responses to warming and elevated CO2. P Natl Acad Sci USA 116:21623–21628

    Article  CAS  Google Scholar 

  • Olano JM, Gonzalez-Munoz N, Arzac A, Rozas V, von Arx G, Delzon S, Garcia-Cervigon AI (2017) Sex determines xylem anatomy in a dioecious conifer: hydraulic consequences in a drier world. Tree Physiol 37:1493–1502

    Article  PubMed  Google Scholar 

  • Parvin S, Uddin S, Tausz-Posch S, Fitzgerald G, Armstrong R, Tausz M (2019) Elevated CO2 improves yield and N2 fixation but not grain N concentration of faba bean (Vicia faba L.) subjected to terminal drought. Environ Exp Bot 165:161–173

    Article  CAS  Google Scholar 

  • Penuelas J, Estiarte M (1998) Can elevated CO2 affect secondary metabolism and ecosystem function? Trend Ecol Evol 13:20–24

    Article  CAS  Google Scholar 

  • Potter C, Bubier J, Crill P, Lafleur P (2001) Ecosystem modeling of methane and carbon dioxide fluxes for boreal forest sites. Can J Forest Res 31:208–223

    CAS  Google Scholar 

  • Randriamanana TR, Nissinen K, Moilanen J, Nybakken L, Julkunen-Tiitio R (2015) Long-term UV-B and temperature enhancements suggest that females of Salix myrsinifolia plants are more tolerant to UV-B than males. Environ Exp Bot 109:296–305

    Article  CAS  Google Scholar 

  • Reddy A, Rasineni G, Raghavendra A (2010) The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Curr Sci India 99:46–57

    CAS  Google Scholar 

  • Rodrigues W et al (2018) Stomatal and photochemical limitations of photosynthesis in coffee (Coffea spp.) plants subjected to elevated temperatures. Crop Pasture Sci 69:317–325

    Article  CAS  Google Scholar 

  • Saleh A, Selim S, Al Jaouni S, Abdelgawad H (2018) CO2 enrichment can enhance the nutritional and health benefits of parsley (Petroselinum crispum L.) and dill (Anethum graveolens L.). Food Chem 269:519–526

    Article  CAS  PubMed  Google Scholar 

  • Shah SRU, Agback P, Lundquist PO (2015) Root morphology and cluster root formation by seabuckthorn (Hippophae rhamnoides L.) in response to nitrogen, phosphorus and iron deficiency. Plant Soil 397:75–91

    Article  Google Scholar 

  • Sharma S, Walia S, Rathore S, Kumar P, Kumar R (2019) Combined effect of elevated CO2 and temperature on growth, biomass and secondary metabolite of Hypericum perforatum L. in a western Himalayan region. J Appl Res Med Aroma 16:100239

    Google Scholar 

  • Sharwood RE, Crous KY, Whitney SM, Ellsworth DS, Ghannoum O (2017) Linking photosynthesis and leaf N allocation under future elevated CO2 and climate warming in Eucalyptus globulus. J Exp Bot 68:1157–1167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stulen I, Denhertog J (1993) Root-growth and functioning under atmospheric CO2 enrichment. Vegetatio 104:99–115

    Article  Google Scholar 

  • Tingey DT, McKane RB, Olszyk DM, Johnson MG, Rygiewicz PT, Lee EH (2003) Elevated CO2 and temperature alter nitrogen allocation in Douglas-fir. Global Change Biol 9:1038–1050

    Article  Google Scholar 

  • Tognetti R (2012) Adaptation to climate change of dioecious plants: Does gender balance matter? Tree Physiol 32:1321–1324

    Article  PubMed  Google Scholar 

  • Vankooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  CAS  Google Scholar 

  • von Caemmerer S (2020) Rubisco carboxylase/oxygenase: from the enzyme to the globe: a gas exchange perspective. J Plant Physiol 252:153240

    Article  Google Scholar 

  • Wang JC, Duan BL, Zhang YB (2012) Effects of experimental warming on growth, biomass allocation, and needle chemistry of Abies faxoniana in even-aged monospecific stands. Plant Ecol 213:47–55

    Article  Google Scholar 

  • Wang B et al (2020) Leaf photosynthesis and stomatal conductance acclimate to elevated [CO2] and temperature thus increasing dry matter productivity in a double rice cropping system. Field Crop Res 248:107735

    Article  Google Scholar 

  • Wiley E, Hoch G, Landhausser SM (2017) Dying piece by piece: carbohydrate dynamics in aspen (Populus tremuloides) seedlings under severe carbon stress. J Exp Bot 68:5221–5232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Peng GQ, Wu CC, Korpelainen H, Li CY (2008) Drought inhibits photosynthetic capacity more in females than in males of Populus cathayana. Tree Physiol 28:1751–1759

    Article  PubMed  Google Scholar 

  • Yu L, Song MY, Xia ZC, Korpelainen H, Niinemets U, Li CY (2019) Elevated temperature differently affects growth, photosynthetic capacity, nutrient absorption and leaf ultrastructure of Abies faxoniana and Picea purpurea under intra- and interspecific competition. Tree Physiol 39:1342–1357

    Article  CAS  PubMed  Google Scholar 

  • Zhang GY, Zhang T, Liu JJ, Zhang JG, He CY (2018) Comprehensive analysis of differentially expressed genes reveals the molecular response to elevated CO2 levels in two sea buckthorn cultivars. Gene 660:122–127

    Article  Google Scholar 

  • Zhao HX, Li YP, Zhang XL, Korpelainen H, Li CY (2012) Sex-related and stage-dependent source-to-sink transition in Populus cathayana grown at elevated CO2 and elevated temperature. Tree Physiol 32:1325–1338

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Funding was provided by the collaborative project between NSFCRCN funded by the National Natural Science Foundation of China (Grant no. 41861134039, 31700536) and by the National Natural Science Foundation of China (No. 31700536).

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Authors and Affiliations

  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041, China

    Yan Su, Hao Jiang, Baoli Duan, Meiyu Liu & Yuanbin Zhang

  2. Jiangsu Lianyungang Environmental Monitoring Center, Lianyungang, 222000, China

    Shuxin Li

  3. University of Chinese Academy of Sciences, Beijing, 100039, China

    Yan Su

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  1. Yan Su
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Su, Y., Li, S., Jiang, H. et al. Sex-specific physiological and growth responses to elevated temperature and CO2 concentration in Chinese seabuckthorn (Hippophae rhamnoides subsp. sinensis Rousi). Acta Physiol Plant 45, 53 (2023). https://doi.org/10.1007/s11738-023-03520-z

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