Abstract
Extreme soil temperatures are the main limitation to the expansion of agriculture. In Brazil, this also affects the second crop, which is usually performed every year. We investigated the influence of soil temperature on the ecophysiology of two plant species with different mechanisms of CO2 assimilation: maize (C4) and bean (C3). The plants, in the vegetative phase, were subjected to three soil temperatures: low (9–12 °C), ambient (25–30 °C), and high (27–42 °C). Our results indicate that both low and high soil temperatures negatively affected the photosynthetic process of the studied plants. The reduction of CO2 assimilation rates under low soil temperature was mainly due to stomatal closure, while under high soil temperatures, it was related to decreased carboxylation rates. Short-term exposure to extreme soil temperatures affects the root system growth and, in maize plants, leads to impaired shoot dry mass accumulation. Besides that, stresses caused by high soil temperature reduced the relative water content of the leaves, causing an increase in leaf temperature and cells rupture.
Similar content being viewed by others
References
Alam B, Nair DB, Jacob J (2005) Low temperature stress modifies the photochemical efficiency of a tropical tree species Hevea brasiliensis: effects of varying concentration of CO2 and photon flux density. Photosynthetica 43:247–252. https://doi.org/10.1007/s11099-005-0040-z
Allakhverdiev SI, Kreslavski VD, Klimov VV et al (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis. https://doi.org/10.1007/s11120-008-9331-0
Arai-Sanoh Y, Ishimaru T, Ohsumi A, Kondo M (2010) Effects of soil temperature on growth and root function in rice. Plant Prod Sci 13:235–242. https://doi.org/10.1626/pps.13.235
Chinthapalli B, Murmu J, Raghavendra AS (2003) Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants. J Exp Bot 54:707–714
Crafts-Brandner SJ, Salvucci ME (2004) Analyzing the impact of high temperature and CO2 on net photosynthesis: biochemical mechanisms, models and genomics. Field Crop Res 90:75–85. https://doi.org/10.1016/j.fcr.2004.07.006
de Nóia Júnior RS, Pezzopane JEM, Cecílio RA et al (2017) Calibration of tdr probe for estimating moisture in different types of substrates. Rev Bras Agric Irrig 11:2132–2140. https://doi.org/10.7127/rbai.v11n800694
Du Y-C, Nose A, Wasano K (1999) Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species. Plant Cell Environ 22:317–324. https://doi.org/10.1046/j.1365-3040.1999.00415.x
Dwyer SA, Ghannoum O, Nicotra A, Von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant Cell Environ 30:53–66. https://doi.org/10.1111/j.1365-3040.2006.01605.x
Eyshi Rezaei E, Webber H, Gaiser T et al (2015) Heat stress in cereals: mechanisms and modelling. Eur J Agron 64:98–113. https://doi.org/10.1016/j.eja.2014.10.003
Fu J, Gates RN, Xu Y, Hu T (2016) Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis following cold stress in Elymus nutans Griseb. J Photochem Photobiol B 163:30–39. https://doi.org/10.1016/j.jphotobiol.2016.08.008
Garruña-Hernández R, Orellana R, Larque-Saavedra A, Canto A (2014) Understanding the physiological responses of a tropical crop (Capsicum chinense Jacq.) at high temperature. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0111402
Godfray HCJ, Beddington JR, Crute IR et al (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818
Govindjee GC, Papageorgiou BC, Biswal B et al (2011) Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation. Curr Sci 101:47–56
Greer DH, Weedon MM (2012) Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate. Plant Cell Environ 35:1050–1064. https://doi.org/10.1111/j.1365-3040.2011.02471.x
Gururani MA, Venkatesh J, Tran LSP et al (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extrem 10:4–10. https://doi.org/10.1016/j.wace.2015.08.001
Hendrickson L, Sharwood R, Ludwig M et al (2007) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59:1789–1798. https://doi.org/10.1093/jxb/erm373
Hikosaka K (2005) Nitrogen partitioning in the photosynthetic apparatus of plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. Plant Cell Physiol 46:1283–1290. https://doi.org/10.1093/pcp/pci137
Koolhaas JM, Bartolomucci A, Buwalda B et al (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291–1301. https://doi.org/10.1016/j.neubiorev.2011.02.003
Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173:519–527. https://doi.org/10.1007/BF00958965
Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620
Makino A, Sage RF (2007) Temperature Response of photosynthesis in transgenic rice transformed with “Sense” or “Antisense” RBCs. Plant Cell Physiol 48:1472–1483. https://doi.org/10.1093/pcp/pcm118
Mathur S, Agrawal D, Jajoo A (2014) Photosynthesis: response to high temperature stress. J Photochem Photobiol B 137:116–126. https://doi.org/10.1016/j.jphotobiol.2014.01.010
Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462. https://doi.org/10.1146/annurev-arplant-042809-112116
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125. https://doi.org/10.1016/j.tibs.2011.11.007
Monroe JD, Storm AR, Badley EM et al (2014) Amylase1 and -Amylase3 are plastidic starch hydrolases in Arabidopsis that seem to be adapted for different thermal, pH, and stress conditions. Plant Physiol 166:1748–1763. https://doi.org/10.1104/pp.114.246421
O’sullivan OS, Heskel MA, Reich PB et al (2017) Thermal limits of leaf metabolism across biomes. Glob Chang Biol 23:209–223. https://doi.org/10.1111/gcb.13477
Oliver SN, Van Dongen JT, Alfred SC et al (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1551. https://doi.org/10.1111/j.1365-3040.2005.01390.x
Pittermann J, Sage RF (2001) The response of the high altitude C(4) grass Muhlenbergia montana (Nutt.) A.S. Hitchc. to long- and short-term chilling. J Exp Bot 52:829–838
Prezotti LC, Gomes JA, Dadalto GG (2007) Manual de recomendação de calagem e adubação para o Estado do Espírito Santo: 5a aproximação. INCAPER, Vitória
Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106. https://doi.org/10.1111/j.1365-3040.2007.01682.x
Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277. https://doi.org/10.1111/j.1365-3040.2005.01324.x
Song L, Chow WS, Sun L et al (2010) Acclimation of photosystem II to high temperature in two Wedelia species from different geographical origins: implications for biological invasions upon global warming. J Exp Bot 61:4087–4096. https://doi.org/10.1093/jxb/erq220
Strand Å, Hurry V, Henkes S et al (1999) Acclimation of Arabidopsis leaves developing at low temperatures. increasing cytoplasmic volume accompanies increased activities of enzymes in the calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1398
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x
Szymańska R, Ślesak I, Orzechowska A, Kruk J (2017) Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot 139:165–177. https://doi.org/10.1016/j.envexpbot.2017.05.002
Wang JZ, Cui LJ, Wang Y, Li JL (2009) Growth, lipid peroxidation and photosynthesis in two tall fescue cultivars differing in heat tolerance. Biol Plant 53:237–242. https://doi.org/10.1007/s10535-009-0045-8
Wang WH, Yi XQ, Han AD et al (2012) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot 63:177–190. https://doi.org/10.1093/jxb/err259
Xiaochuang C, Chu Z, Lianfeng Z et al (2017) Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics, and photosynthesis. Plant Physiol Biochem 112:251–260. https://doi.org/10.1016/j.plaphy.2017.01.008
Yamori W, Noguchi K, Hikosaka K, Terashima I (2010) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152:388–399. https://doi.org/10.1104/pp.109.145862
Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117. https://doi.org/10.1007/s11120-013-9874-6
Zhu J, Zhang K-X, Wang W-S et al (2015) Low Temperature inhibits root growth by reducing auxin accumulation via ARR1/12. Plant Cell Physiol 56:727–736. https://doi.org/10.1093/pcp/pcu217
Acknowledgements
We acknowledge State of Espírito Santo Research Foundation (FAPES) Grant Number 65768051/14 for fellowships granted and for financial support of this research.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nóia Júnior, R.S., do Amaral, G.C., Pezzopane, J.E.M. et al. Ecophysiology of C3 and C4 plants in terms of responses to extreme soil temperatures. Theor. Exp. Plant Physiol. 30, 261–274 (2018). https://doi.org/10.1007/s40626-018-0120-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-018-0120-7