Abstract
The maternal carbon dioxide environment affected the responses of offspring to elevated carbon dioxide with regard to stomatal density, photosynthesis and yield.
AbstractSection AbstractThe responses of crops to rising carbon dioxide concentration ([CO2]) are often validated using single-generation short-term experiments. However, the transgenerational effects of elevated [CO2] on rice growth have received little attention. Here, we set up ambient [CO2] (a[CO2]) and elevated [CO2] (e[CO2], a[CO2] + 200 µmol mol−1) treatments using open-top chamber (OTC). Rice was cultivated in different [CO2] treatments over five growing seasons in 2016–2020. Beginning in 2017, rice seeds harvested in the previous year under a[CO2] and e[CO2] conditions were planted in their respective growing environments. In 2021, seedlings derived from a[CO2] maternal treatment (a[CO2]m) and e[CO2] maternal treatment (e[CO2]m) were planted with both a[CO2] offspring (a[CO2]o) and e[CO2] offspring (e[CO2]o) conditions to investigate the transgenerational effects of e[CO2]. Leaf gas exchange and grain yield under different conditions were determined in 2021. The results showed that light-saturated net photosynthesis (Asat) and stomatal conductance of offspring from e[CO2]m were significantly lower at the heading and grain-filling stages under e[CO2]o compared with a[CO2]m, and the corresponding stomatal density was also significantly lower. Moreover, Asat was positively correlated with stomatal density. These results suggest that transgenerational effects induce a decrease in stomatal density and thus cause a lower benefit of Asat from e[CO2]o. These findings contribute new insights into predicting crop growth and yield in the future.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The datasets are available from the corresponding author on reasonable request.
References
Ainsworth EA (2008) Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Glob Change Biol 14:1642–1650. https://doi.org/10.1111/j.1365-2486.2008.01594.x
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol 165:351–371. https://doi.org/10.1111/j.1469-8137.2004.01224.x
Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant Cell Environ 30:258–270. https://doi.org/10.1111/j.1365-3040.2007.01641.x
Bezemer TM, Thompson LJ, Jones TH (1998) Poa annua shows inter-generational differences in response to elevated CO2. Glob Change Biol 4:687–691. https://doi.org/10.1046/j.1365-2486.1998.00184.x
Bunce JA (2001) Direct and acclimatory responses of stomatal conductance to elevated carbon dioxide in four herbaceous crop species in the field. Glob Change Biol 7:323–331. https://doi.org/10.1046/j.1365-2486.2001.00406.x
Cai C, Li G, Yang H, Yang J, Liu H, Struik PC, Luo W, Yin X, Di L, Guo X, Jiang W, Si C, Pan G, Zhu J (2018) Do all leaf photosynthesis parameters of rice acclimate to elevated CO2, elevated temperature, and their combination, in FACE environments? Glob Change Biol 24:1685–1707. https://doi.org/10.1111/gcb.13961
Caine RS, Yin X, Sloan J, Harrison EL, Mohammed U, Fulton T, Biswal AK, Dionora J, Chater CC, Coe RA, Bandyopadhyay A, Murchie EH, Swarup R, Quick WP, Gray JE (2019) Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221:371–384. https://doi.org/10.1111/nph.15344
Cao P, Sun W, Huang Y, Yang J, Yang K, Lv C, Wang Y, Yu L, Hu Z (2020) Effects of elevated CO2 concentration and nitrogen application levels on the accumulation and translocation of non-structural carbohydrates in japonica rice. Sustainability. https://doi.org/10.3390/su12135386
Del Pozo A, Perez P, Morcuende R, Alonso A, Martinez-Carrasco R (2005) Acclimatory responses of stomatal conductance and photosynthesis to elevated CO2 and temperature in wheat crops grown at varying levels of N supply in a Mediterranean environment. Plant Sci 169:908–916. https://doi.org/10.1016/j.plantsci.2005.06.009
Ding Y, Liu N, Virlouvet L, Riethoven J-J, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. https://doi.org/10.1186/1471-2229-13-229
Dobert RC, Blevins DG (1993) Effect of seed size and plant growth on nodulation and nodule development in lima bean (Phaseolus lunatus L.). Plant Soil 148:11–19. https://doi.org/10.1007/BF02185380
Engineer CB, Hashimoto-Sugimoto M, Negi J, Israelsson-Nordstrom M, Azoulay-Shemer T, Rappel W-J, Iba K, Schroeder JI (2016) CO2 Sensing and CO2 peculation of stomatal conductance: advances and open questions. Trends Plant Sci 21:16–30. https://doi.org/10.1016/j.tplants.2015.08.014
Field KJ, Duckett JG, Cameron DD, Pressel S (2015) Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Ann Bot 115:915–922. https://doi.org/10.1093/aob/mcv021
Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136. https://doi.org/10.1126/science.1148766
Groot MP, Kubisch A, Ouborg NJ, Pagel J, Schmid KJ, Vergeer P, Lampei C (2017) Transgenerational effects of mild heat in Arabidopsis thaliana show strong genotype specificity that is explained by climate at origin. New Phytol 215:1221–1234. https://doi.org/10.1111/nph.14642
Hasegawa T, Sakai H, Tokida T, Nakamura H, Zhu C, Usui Y, Yoshimoto M, Fukuoka M, Wakatsuki H, Katayanagi N, Matsunami T, Kaneta Y, Sato T, Takakai F, Sameshima R, Okada M, Mae T, Makino A (2013) Rice cultivar responses to elevated CO2 at two free-air CO2 enrichment (FACE) sites in Japan. Funct Plant Biol 40:148–159. https://doi.org/10.1071/FP12357
Hatfield JL, Boote KJ, Kimball BA, Ziska LH, Izaurralde RC, Ort D, Thomson AM, Wolfe D (2011) Climate impacts on agriculture: Implications for crop production. Agron J 103:351–370. https://doi.org/10.2134/agronj2010.0303
Herman JJ, Sultan SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front Plant Sci. https://doi.org/10.3389/fpls.2011.00102
IPCC (2013) Summary for policymakers. In: Stocker TF et al (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Klironomos JN, Allen MF, Rillig MC, Piotrowski J, Makvandi-Nejad S, Wolfe BE, Powell JR (2005) Abrupt rise in atmospheric CO2 overestimates community response in a model plant-soil system. Nature 433:621–624. https://doi.org/10.1038/nature03268
Lau JA, Peiffer J, Reich PB, Tiffin P (2008) Transgenerational effects of global environmental change: long-term CO2 and nitrogen treatments influence offspring growth response to elevated CO2. Oecologia 158:141–150. https://doi.org/10.1007/s00442-008-1127-6
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876. https://doi.org/10.1093/jxb/erp096
Leakey ADB, Ainsworth EA, Bernacchi CJ, Zhu X, Long SP, Ort DR (2012) Photosynthesis in a CO2-rich atmosphere. In: Eaton-Rye J, Tripathy B, Sharkey T (eds) Photosynthesis: advances in photosynthesis and respiration. Springer, Dordrecht, pp 733–768
Li X, Khan A, Lv Z, Fang L, Jiang D, Liu F (2019) Effect of multigenerational exposure to elevated atmospheric CO2 concentration on grain quality in wheat. Environ Exp Bot 157:310–319. https://doi.org/10.1016/j.envexpbot.2018.10.028
Liao Z, Yu H, Duan J, Yuan K, Yu C, Meng X, Kou L, Chen M, Jing Y, Liu G, Smith SM, Li J (2019) SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nat Commun 10:2738. https://doi.org/10.1038/s41467-019-10667-2
Lin JX, Jach ME, Ceulemans R (2001) Stomatal density and needle anatomy of Scots pine (Pinus sylvestris) are affected by elevated CO2. New Phytol 150:665–674. https://doi.org/10.1046/j.1469-8137.2001.00124.x
Lodge RJ, Dijkstra P, Drake BG, Morison JIL (2001) Stomatal acclimation to increased CO2 concentration in a Florida scrub oak species Quercus myrtifolia Willd. Plant Cell Environ 24:77–88. https://doi.org/10.1046/j.1365-3040.2001.00659.x
Lv C, Huang Y, Sun W, Yu L, Zhu J (2020) Response of rice yield and yield components to elevated CO2: a synthesis of updated data from FACE experiments. Eur J Agron. https://doi.org/10.1016/j.eja.2019.125961
Martinez-Carrasco R, Perez P, Morcuende R (2005) Interactive effects of elevated CO2, temperature and nitrogen on photosynthesis of wheat grown under temperature gradient tunnels. Environ Exp Bot 54:49–59. https://doi.org/10.1016/j.envexpbot.2004.05.004
Mishra Y, Rawat R, Rana PK, Sonkar MK, Mohammad N (2014) Effect of seed mass on emergence and seedling development in Pterocarpus marsupium Roxb. J For Res 25:415–418. https://doi.org/10.1007/s11676-014-0469-7
Reich PB, Hobbie SE, Lee TD, Pastore MA (2018) Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment. Science 360:317–320. https://doi.org/10.1126/science.aas9313
Reid CD, Maherali H, Johnson HB, Smith SD, Wullschleger SD, Jackson RB (2003) On the relationship between stomatal characters and atmospheric CO2. Geophys Res Lett. https://doi.org/10.1029/2003GL017775
Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol 198:757–764. https://doi.org/10.1111/nph.12186
Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103. https://doi.org/10.1111/j.1469-8137.2006.01818.x
Tricker PJ, Trewin H, Kull O, Clarkson GJJ, Eensalu E, Tallis MJ, Colella A, Doncaster CP, Sabatti M, Taylor G (2005) Stomatal conductance and not stomatal density determines the long-term reduction in leaf transpiration of poplar in elevated CO2. Oecologia 143:652–660. https://doi.org/10.1007/s00442-005-0025-4
Turgut-Kara N, Arikan B, Celik H (2020) Epigenetic memory and priming in plants. Genetica 148:47–54. https://doi.org/10.1007/s10709-020-00093-4
Upadhaya K, Pandey H, Law PS (2007) The effect of seed mass on germination, seedling survival and growth in Prunus jenkinsii Hook.f. and Thoms. Turk J Bot 31:31–36
von Caemmerer S, Evans JR (2010) Enhancing C3 photosynthesis. Plant Physiol 154:589–592. https://doi.org/10.1104/pp.110.160952
Vrablova M, Hronkova M, Vrabl D, Kubasek J, Santrucek J (2018) Light intensity-regulated stomatal development in three generations of Lepidium sativum. Environ Exp Bot 156:316–324. https://doi.org/10.1016/j.envexpbot.2018.09.012
Wang L, Feng ZZ, Schjoerring JK (2013) Effects of elevated atmospheric CO2 on physiology and yield of wheat (Triticum aestivum L.): a meta-analytic test of current hypotheses. Agric Ecosyst Environ 178:57–63. https://doi.org/10.1016/j.agee.2013.06.013
Wang J, Wang C, Chen N, Xiong Z, Wolfe D, Zou J (2015) Response of rice production to elevated [CO2] and its interaction with rising temperature or nitrogen supply: a meta-analysis. Clim Change 130:529–543. https://doi.org/10.1007/s10584-015-1374-6
Wang Z, Baskin JM, Baskin CC, Yang X, Liu G, Ye X, Huang Z, Cornelissen JHC (2022) Great granny still ruling from the grave: phenotypical response of plant performance and seed functional traits to salt stress affects multiple generations of a halophyte. J Ecol 110:117–128. https://doi.org/10.1111/1365-2745.13789
WMO (2020) The state of greenhouse in the atmosphere based on global observations through 2019. WMO Greenhouse Gas Bulletin, No. 16, 23 November 2020
Wong JM, Johnson KM, Kelly MW, Hofmann G (2018) Transcriptomics reveal transgenerational effects in purple sea urchin embryos: adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels. Mol Ecol 27:1120–1137. https://doi.org/10.1111/mec.14503
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618. https://doi.org/10.1038/327617a0
Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325. https://doi.org/10.1093/jxb/ern185
Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00657
Yan WM, Zhong YQW, Shangguan ZP (2017) Contrasting responses of leaf stomatal characteristics to climate change: a considerable challenge to predict carbon and water cycles. Glob Change Biol 23:3781–3793. https://doi.org/10.1111/gcb.13654
Yang J, Cao P, Yang K, Lyu C, Wang Y, Sun W, Yu L, Hu Z, Huang Y (2021) Effects of source-sink manipulation on the accumulation and translocation of non-structural carbohydrates in stems and sheaths of japonica rice under elevated CO2 concentration and different nitrogen fertilization levels. Chin J Ecol 40:615–626
Zhou Y, Jiang X, Schaub M, Wang X, Han J, Han S-J, Li M-H (2013) Ten-year exposure to elevated CO2 increases stomatal number of Pinus koraiensis and P. sylvestriformis needles. Eur J For Res 132:899–908. https://doi.org/10.1007/s10342-013-0728-8
Acknowledgements
This work was supported by National Natural Science Foundation of China (Grant Nos. 41530533, 31972937, 42071023) and the Youth Fund of the Ministry of Education Laboratory for Earth Surface Processes, Peking University. We sincerely thank Dr. Yao Huang at Institute of Botany, Chinese Academy of Sciences, China for his guidance and help in experiment and sampling.
Author information
Authors and Affiliations
Contributions
CL and YW conceived the ideas. ZH provided experimental platform. CL performed data collection, statistical analysis and wrote the first draft of the manuscript. JW drew the working model. CL, ZH and YW commented on the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Fig. S1
Effects of offspring [CO2] treatments on the actual quantum efficiency of PSII (ΦPSII) (a) and actual photochemical efficiency of PSII (Fv′/Fm′) (b) of rice derived from maternal a[CO2] and e[CO2] treatments at different growth stages (jointing, heading and grain-filling stages). Values are the mean ± SE (n = 9). a[CO2] and e[CO2] represent ambient and elevated CO2 concentrations, respectively. [CO2]o and [CO2]m indicate offspring and maternal CO2 growth environments, respectively. * represents significance at a probability level of p < 0.05. ns indicates no statistical significance. Fig. S2 Effects of offspring [CO2] treatments on intercellular [CO2] (Ci) of rice derived from maternal a[CO2] and e[CO2] treatments at different growth stages (jointing, heading and grain-filling stages). Values are the mean ± SE (n = 9). a[CO2] and e[CO2] represent ambient and elevated CO2 concentrations, respectively. [CO2]o and [CO2]m indicate offspring and maternal CO2 growth environments, respectively. Fig. S3 Correlation of stomatal conductance (gs) (a) and light-saturated net photosynthesis (Asat) (b) with stomatal length at heading stage. a[CO2]o and e[CO2]o represent offspring ambient and elevated CO2 concentrations, respectively. Fig. S4 Panicle number of plants from ambient maternal [CO2] (a[CO2]m) and elevated maternal [CO2] (e[CO2]m) conditions under ambient (a[CO2]o) and elevated offspring CO2 treatment (e[CO2]o). Fig. S5 Relative stomatal density of flag leaves of plants from ambient maternal [CO2] (a[CO2]m) and elevated maternal [CO2] (e[CO2]m) conditions under elevated offspring CO2 treatment in 2018–2021. *** represents significance at a probability level of p < 0.001. ns indicates no statistical significance. Fig. S6 Heat map of the differentially expressed genes in photosynthesis and related processes. a[CO2] and e[CO2] represent ambient and elevated CO2 concentration, respectively. [CO2]o and [CO2]m indicate offspring and maternal CO2 growth environment, respectively. Nine flag leaves were randomly selected for each treatment and frozen in liquid nitrogen and stored at -80 °C. Total RNA was extracted from a mixture of nine leaves using the TRIzol Reagent Mini Kit (Qiagen) following the manufacturer’s instructions. Sequencing was carried out using an Illumina HiSeq instrument according to manufacturer’s instructions (Illumina, San Diego, CA, USA). Gene-expression level was calculated and normalized to fragments per kilobase of transcript per million mapped reads. Fig. S7 Relative methylation modification levels of genes that change simultaneously at the transcription level and methylation level in plants from different maternal [CO2] environments (ambient maternal [CO2]: a[CO2]m; elevated maternal [CO2]: e[CO2]m) under different offspring [CO2] treatments (ambient offspring [CO2]: a[CO2]o; elevated offspring [CO2]: e[CO2]o). The genomic DNA was extracted from a mixture of nine leaves using the DNeasy Plant Mini Kit (Qiagen). Bisulfite conversion of DNA was carried out using the Epitect Bisulfite Kit (Qiagen) according to manufacturer’s instructions. Bisulfite-treated DNA was sequenced to determine the DNA methylation level. (DOCX 1741.7 kb)
Rights and permissions
About this article
Cite this article
Lv, C., Hu, Z., Wei, J. et al. Transgenerational effects of elevated CO2 on rice photosynthesis and grain yield. Plant Mol Biol 110, 413–424 (2022). https://doi.org/10.1007/s11103-022-01294-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-022-01294-5