Abstract
Key Message
A novel non-steady-state kinematic analysis shows differences in cell division and expansion determining a better recovery from a 3-day cold spell in emerged compared to non-emerged maize leaves.
Abstract
Zea mays is highly sensitive to chilling which frequently occurs during its seedling stage. Although the direct effect of chilling is well studied, the mechanisms determining the subsequent recovery are still unknown. Our goal is to determine the cellular basis of the leaf growth response to chilling and during recovery of leaves exposed before or after their emergence. We first studied the effect of a 3-day cold spell on leaf growth at the plant level. Then, we performed a kinematic analysis to analyse the dynamics of cell division and elongation during recovery of the 4th leaf after exposure to cold before or after emergence. Our results demonstrated cold more strongly reduced the final length of non-emerged than emerged leaves (− 13 vs. − 18%). This was not related to growth differences during cold, but a faster and more complete recovery of the growth of emerged leaves. This difference was due to a higher cell division rate on the 1st and a higher cell elongation rate on the 2nd day of recovery, respectively. The dynamics of cell division and expansion during recovery determines developmental stage-specific differences in cold tolerance of maize leaves.
Similar content being viewed by others
Data availability
None.
References
Ade-Ademilua OE, Botha CEJ, Strasser RJ (2005) A re-evaluation of plastochron index determination in peas—a case for using leaflet length. S Afr J Bot 71:76–80
Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42
Aroca R, Vernieri P, Irigoyen JJ, Sánchez-Dı́az M, Tognoni F, Pardossi A. (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165:671–679
Atkinson LJ, Sherlock DJ, Atkin OK (2015) Source of nitrogen associated with recovery of relative growth rate in Arabidopsis thaliana acclimated to sustained cold treatment. Plant Cell Environ 38:1023–1034
Avila LM, Obeidat W, Earl H, Niu X, Hargreaves W, Lukens L (2018) Shared and genetically distinct Zea mays transcriptome responses to ongoing and past low temperature exposure. BMC Genomics 19:761
Avramova V, AbdElgawad H, Zhang Z, Fotschki B, Casadevall R, Vergauwen L, Knapen D, Taleisnik E, Guisez Y, Asard H et al (2015) Drought induces distinct growth response, protection, and recovery mechanisms in the maize leaf growth zone. Plant Physiol 169:1382–1396
Aydinoglu F (2020) Elucidating the regulatory roles of microRNAs in maize (Zea mays L.) leaf growth response to chilling stress. Planta 251:38.
Bashline L, Lei L, Li S, Gu Y (2014) Cell wall, cytoskeleton, and cell expansion in higher plants. Mol Plant 7:586–600
Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526
Beemster GTS, Masle J (1996) The role of apical development around the time of leaf initiation in determining leaf width at maturity in wheat seedlings (Triticum aestivum L.) with impeded roots. J Exp Bot 47:1679–1688
Ben Haj Salah H, Tardieu F (1996) Quantitative analysis of the combined effects of temperature, evaporative demand and light on leaf elongation rate in well-watered field and laboratory-grown maize plants. J Exp Bot 47:1689–1698
Ben-Haj-Salah H, Tardieu F (1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length (analysis of the coordination between cell division and cell expansion). Plant Physiol 109:861–870
Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet MGG 262:534–542
Bernstein N, Lauchli A, Silk WK (1993) Kinematics and dynamics of sorghum (Sorghum bicolor L.) leaf development at various Na/Ca salinities (I. elongation growth). Plant Physiol 103:1107–1114
Bertels J, Beemster GTS (2020) leafkin—An R package for automated kinematic data analysis of monocot leaves. Quant Plant Biol 1
Birch C, Vos J, Kiniry J, Bos HJ, Elings A (1998) Phyllochron responds to acclimation to temperature and irradiance in maize. Field Crop Res 59:187–200
Brüggemann W, van der Kooij TAW, van Hasselt PR (1992) Long-term chilling of young tomato plants under low light and subsequent recovery: I. Growth, development and photosynthesis. Planta 186:172–178
Burnett AC, Kromdijk J (2022) Can we improve the chilling tolerance of maize photosynthesis through breeding? J Exp Bot erac045.
Chapin FS III (1991) Integrated responses of plants to stress: a centralized system of physiological responses. Bioscience 41:29–36
Chmielowska-Bąk J, Deckert J (2021) Plant recovery after metal stress—a review. Plants 10:450
Cholakova R, Vassilev A (2017) Effect of chilling stress on the photosynthetic performance of young plants from two maize (Zea mays) hybrids. CBU Int Conf Proc 5:1118–1123
Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, Storme V, Clement L, Gonzalez N, Inzé D (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol 167:800–816
Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67:463–476
De Vos D, Nelissen H, AbdElgawad H, Prinsen E, Broeckhove J, Inzé D, Beemster GTS (2020) How grass keeps growing: an integrated analysis of hormonal crosstalk in the maize leaf growth zone. New Phytol 225:2513–2525
DeRidder BP, Crafts-Brandner SJ (2008) Chilling stress response of postemergent cotton seedlings. Physiol Plant 134:430–439
Erickson RO (1976) Modeling of plant growth. Annu Rev Plant Physiol 27:407–434
Erickson RO, Michelini FJ (1957) The Plastochron Index. Am J Bot 44:297–305
Farooq M, Aziz T, Wahid A, Lee D-J, Siddique KHM (2009) Chilling tolerance in maize: agronomic and physiological approaches. Crop Pasture Sci 60:501–516
Fina J, Casadevall R, AbdElgawad H, Prinsen E, Markakis MN, Beemster GTS, Casati P (2017) UV-B inhibits leaf growth through changes in growth regulating factors and gibberellin levels. Plant Physiol 174:1110–1126
Fiorani F, Beemster G (2006) Quantitative analyses of cell division in plants. Plant Mol Biol 60:963–979
Frei O (2000) Changes in yield physiology of corn as a result of breeding in northern Europe. Maydica 45:173–183
Garbero M, Andrade A, Reinoso H, Fernández B, Cuesta C, Granda V, Escudero C, Abdala G, Pedranzani H (2012) Differential effect of short-term cold stress on growth, anatomy, and hormone levels in cold-sensitive versus -resistant cultivars of Digitaria eriantha. Acta Physiol Plant 34:2079–2091
Giauffret C, Bonhomme R, Derieux M (1995) Genotypic differences for temperature response of leaf appearance rate and leaf elongation rate in field-grown maize. Agronomie 2(15):123–137
Gómez LD, Vanacker H, Buchner P, Noctor G, Foyer CH (2004) Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134:1662–1671
Granier C, Tardieu F (1998) Is thermal time adequate for expressing the effects of temperature on sunflower leaf development? Plant Cell Environ 21:695–703
Granier C, Tardieu F (2000) Sunflower leaf growth under changing environmental conditions. OCL Oleagineux Corps Gras Lipides 7:219–228
Greaves JA (1996) Improving suboptimal temperature tolerance in maize- the search for variation. J Exp Bot 47:307–323
Green PB (1976) Growth and cell pattern formation on an axis: critique of concepts, terminology, and modes of study. Bot Gaz 137:187–202
Hasanfard A, Rastgoo M, Izadi Darbandi E, Nezami A, Chauhan BS (2021) Regeneration capacity after exposure to freezing in wild oat (Avena ludoviciana Durieu.) and turnipweed (Rapistrum rugosum (L.) All.) in comparison with winter wheat. Environ Exp Bot 181:104271
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
Lainé CMS, AbdElgawad H, Beemster GTS (2023) A meta-analysis reveals differential sensitivity of cold stress responses in the maize leaf. Plant Cell Environ 8:2432. https://doi.org/10.1111/pce.14608
Louarn G, Andrieu B, Giauffret C (2010) A size-mediated effect can compensate for transient chilling stress affecting maize (Zea mays) leaf extension. New Phytol 187:106–118
Marowa P, Ding A, Kong Y (2016) Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep 35:949–965
Meicenheimer RD (2014) The plastochron index: still useful after nearly six decades. Am J Bot 101:1821–1835
Miedema P (1982) The effects of low temperature on Zea mays. In: Brady NC (ed) Advances in agronomy. Academic Press, pp 93–128
Muller B, Reymond M, Tardieu F (2001) The elongation rate at the base of a maize leaf shows an invariant pattern during both the steady-state elongation and the establishment of the elongation zone. J Exp Bot 52:1259–1268
Munns R, Passioura JB, Guo J, Chazen O, Cramer GR (2000) Water relations and leaf expansion: importance of time scale. J Exp Bot 51:1495–1504
Pablo J, Clerget B, Bueno C, Dionora J, Domingo A, Guzman C, Aguilar E, Cadiz N, Sta Cruz P (2022) Phyllochron duration and changes through rice development shape the vertical leaf size profile. https://doi.org/10.1101/2022.03.12.484079
Parent B, Conejero G, Tardieu F (2009) Spatial and temporal analysis of non-steady elongation of rice leaves. Plant Cell Environ 32:1561–1572
Pettigrew W (2002) Improved yield potential with an early planting cotton production system. Agron J 94(5):997
Plancade S, Marchadier E, Huet S, Ressayre A, Noûs C, Dillmann C (2023) A successive time-to-event model of phyllochron dynamics for hypothesis testing: application to the analysis of genetic and environmental effects in maize. Plant Methods 19:54
Podgórska A, Burian M, Gieczewska K, Ostaszewska-Bugajska M, Zebrowski J, Solecka D, Szal B (2017) Altered cell wall plasticity can restrict plant growth under ammonium nutrition. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01344
Powles S, Berry J, Björkman O (2006) Interaction between light and chilling temperature on the inhibition of photosynthesis in chilling-sensitive plants*. Plant Cell Environ 6:117–123
Rankenberg T, Geldhof B, van Veen H, Holsteens K, de Poel BV, Sasidharan R (2021) Age-dependent abiotic stress resilience in plants. Trends Plant Sci 26:692–705
Ratajczak K, Sulewska H, Panasiewicz K, Faligowska A, Szymańska G (2023) Phytostimulator application after cold stress for better maize (Zea mays L.) plant recovery. Agriculture 13:569
Riva-Roveda L, Escale B, Giauffret C, Périlleux C (2016) Maize plants can enter a standby mode to cope with chilling stress. BMC Plant Biol 16:212
Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438
Salesse-Smith CE, Sharwood RE, Busch FA, Stern DB (2020) Increased Rubisco content in maize mitigates chilling stress and speeds recovery. Plant Biotechnol J 18:1409–1420
Silk WK (1992) Steady form from changing cells. Int J Plant Sci 153:S49–S58
Silk WK, Erickson RO (1979) Kinematics of plant growth. J Theor Biol 76:481–501
Sprangers K, Avramova V, Beemster GTS (2016) Kinematic analysis of cell division and expansion: quantifying the cellular basis of growth and sampling developmental zones in Zea mays leaves. JoVE. https://doi.org/10.3791/54887
Toda K, Takahashi R, Iwashina T, Hajika M (2011) Difference in chilling-induced flavonoid profiles, antioxidant activity and chilling tolerance between soybean near-isogenic lines for the pubescence color gene. J Plant Res 124:173–182
Vilonen L, Ross M, Smith MD (2022) What happens after drought ends: synthesizing terms and definitions. New Phytol 235:420–431
Wang JY (1960) A critique of the heat unit approach to plant response studies. Ecology 41:785–790
West G, Inzé D, Beemster GTS (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058
Yeung E, van Veen H, Vashisht D, Sobral Paiva AL, Hummel M, Rankenberg T, Steffens B, Steffen-Heins A, Sauter M, de Vries M et al (2018) A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana. Proc Natl Acad Sci 115:E6085–E6094
Zhou X, Muhammad I, Lan H, Xia C (2022) Recent advances in the analysis of cold tolerance in maize. Front Plant Sci 13:866034
Acknowledgements
This work has been supported by The University Research Fund (BOF) with a PhD fellowship. The authors thank Senne Note who contributed to data generation.
Funding
This work was supported by The University Research Fund (BOF) from the University of Antwerp [Grant no. FFB190218].
Author information
Authors and Affiliations
Contributions
CL performed the data analysis and wrote the paper. HAE and GB conceived the idea, supervised the analyses and contributed to the writing.
Corresponding authors
Ethics declarations
Conflict of interest
None.
Additional information
Communicated by Jo Hepworth.
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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lainé, C.M.S., AbdElgawad, H. & Beemster, G.T.S. Cellular dynamics in the maize leaf growth zone during recovery from chilling depends on the leaf developmental stage. Plant Cell Rep 43, 38 (2024). https://doi.org/10.1007/s00299-023-03116-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00299-023-03116-4