Diel leaf growth of rapeseed at critically low temperature under winter field conditions
S. Nagelmüller A B C , S. Yates A and A. Walter A
+ Author Affiliations
- Author Affiliations
A Institute of Agricultural Sciences, Swiss Federal Institute of Technology, Universitätstrasse 2, 8092 Zurich, Switzerland.
B Institute of Botany, Department of Environmental Sciences, University of Basel, Schönbeinstrasse 6, 4056 Basel, Switzerland.
C Corresponding author. Email: sebastian.nagelmueller@usys.ethz.ch
Functional Plant Biology 45(11) 1110-1118 https://doi.org/10.1071/FP17337
Submitted: 28 November 2017 Accepted: 23 April 2018 Published: 17 May 2018
Abstract
Growth and development of winter crops is strongly limited by low temperature during winter. Monitoring the temporal dynamics and thermal limits of leaf growth in that period can give important insights into the growth physiology at low temperature, crop management and future breeding traits for winter crops. In this study, we focussed on winter rapeseed as a model, dicotyledonous winter crop to study leaf growth under natural winter field conditions. Leaf growth was measured using a high-resolution marker based image sequence analysis method and the results were evaluated in the context of environmental conditions. Leaves stopped growing at a base temperature of 0°C. Above ~4°C, leaves grew with a diel (24 h) growth rhythm, which is typically known for dicots at thermally non-limiting growth conditions. Relative leaf growth rates at temperatures above this 4°C threshold were higher at night and showed a pronounced depression during the day, which we could describe by a model based on the environmental factors vapour pressure deficit (VPD), temperature and light with VPD exerting the strongest negative effect on leaf growth. We conclude that leaf growth of the selected model species at low temperatures shows a transition between pronounced environmental regulation and a superposition of environmental and internal, possibly circadian-clock-dependent regulation.
Additional keywords: dicotyledon, growth rhythm, image sequence analysis, low-temperature stress, marker tracking, modeling, modelling, plant growth, vapor pressure deficit, vapour pressure deficit.
References
Abtew W, Melesse A (2013) Vapor pressure calculation methods. In ‘Evaporation and evapotranspiration’. pp. 53–62. (Springer: Dordrecht, The Netherlands)Salah HBH, 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. Journal of Experimental Botany 47, 1689–1698.
| 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.Crossref | GoogleScholarGoogle Scholar |
Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiology 147, 263–279.
| Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome.Crossref | GoogleScholarGoogle Scholar |
Boese SR, Huner NP (1990) Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. Plant Physiology 94, 1830–1836.
| Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Carter TR (1998) Changes in the thermal growing season in Nordic countries during the past century and prospects for the future. Agricultural and Food Science 7, 161–179.
Chouard P (1960) Vernalization and its relations to dormancy. Annual Review of Plant Physiology 11, 191–238.
| Vernalization and its relations to dormancy.Crossref | GoogleScholarGoogle Scholar |
Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biology 9, R130
| Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.Crossref | GoogleScholarGoogle Scholar |
Durand JL, Onillon B, Schnyder H, Rademacher I (1995) Drought effects on cellular and spatial parameters of leaf growth in tall fescue. Journal of Experimental Botany 46, 1147–1155.
| Drought effects on cellular and spatial parameters of leaf growth in tall fescue.Crossref | GoogleScholarGoogle Scholar |
Farré EM (2012) The regulation of plant growth by the circadian clock. Plant Biology 14, 401–410.
| The regulation of plant growth by the circadian clock.Crossref | GoogleScholarGoogle Scholar |
Frich P, Alexander LV, Della-Marta P, Gleason B, Haylock M, Klein Tank AMG, Peterson T (2002) Observed coherent changes in climatic extremes during the second half of the twentieth century. Climate Research 19, 193–212.
| Observed coherent changes in climatic extremes during the second half of the twentieth century.Crossref | GoogleScholarGoogle Scholar |
Gallagher JN, Biscoe PV, Wallace JS (1979) Field studies of cereal leaf growth. IV. Winter wheat leaf extension in relation to temperature and leaf water status. Journal of Experimental Botany 30, 657–668.
| Field studies of cereal leaf growth. IV. Winter wheat leaf extension in relation to temperature and leaf water status.Crossref | GoogleScholarGoogle Scholar |
Grieder C, Hund A, Walter A (2015) Image based phenotyping during winter: a powerful tool to assess wheat genetic variation in growth response to temperature. Functional Plant Biology 42, 387–396.
| Image based phenotyping during winter: a powerful tool to assess wheat genetic variation in growth response to temperature.Crossref | GoogleScholarGoogle Scholar |
Gu HH, Hagberg P, Zhou WJ (2004) Cold pretreatment enhances microspore embryogenesis in oilseed rape (Brassica napus L.). Plant Growth Regulation 42, 137–143.
| Cold pretreatment enhances microspore embryogenesis in oilseed rape (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |
Hodgson AS (1978) Rapeseed adaptation in northern New South Wales. I. Phenological responses to vernalization, temperature and photoperiod by annual and biennial cultivars of Brassica campestris L., Brassica napus L. and wheat cv. Timgalen. Crop and Pasture Science 29, 693–710.
| Rapeseed adaptation in northern New South Wales. I. Phenological responses to vernalization, temperature and photoperiod by annual and biennial cultivars of Brassica campestris L., Brassica napus L. and wheat cv. Timgalen.Crossref | GoogleScholarGoogle Scholar |
Kacperska A, Kulesza L (1987) Frost resistance of winter rape leaves as related to the changes in water potential and growth capability. Physiologia Plantarum 71, 483–488.
| Frost resistance of winter rape leaves as related to the changes in water potential and growth capability.Crossref | GoogleScholarGoogle Scholar |
Kacperska A, Szaniawski RK (1993) Frost resistance and water status of winter rape leaves as affected by differential shoot/root temperature. Physiologia Plantarum 89, 775–782.
| Frost resistance and water status of winter rape leaves as affected by differential shoot/root temperature.Crossref | GoogleScholarGoogle Scholar |
Körner C (2008) Winter crop growth at low temperature may hold the answer for alpine treeline formation. Plant Ecology & Diversity 1, 3–11.
| Winter crop growth at low temperature may hold the answer for alpine treeline formation.Crossref | GoogleScholarGoogle Scholar |
Maciejewska U, Kacperska A (1987) Changes in the level of oxidized and reduced pyridine nucleotides during cold acclimation of winter rape plants. Physiologia Plantarum 69, 687–691.
| Changes in the level of oxidized and reduced pyridine nucleotides during cold acclimation of winter rape plants.Crossref | GoogleScholarGoogle Scholar |
Mendham NJ, Shipway PA, Scott RK (1981) The effects of delayed sowing and weather on growth, development and yield of winter oil-seed rape (Brassica napus). Journal of Agricultural Science 96, 389–416.
| The effects of delayed sowing and weather on growth, development and yield of winter oil-seed rape (Brassica napus).Crossref | GoogleScholarGoogle Scholar |
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397, 659
| Growing season extended in Europe.Crossref | GoogleScholarGoogle Scholar |
Mielewczik M, Friedli M, Kirchgessner N, Walter A (2013) Diel leaf growth of soybean: a novel method to analyze two-dimensional leaf expansion in high temporal resolution based on a marker tracking approach (Martrack Leaf). Plant Methods 9, 30
| Diel leaf growth of soybean: a novel method to analyze two-dimensional leaf expansion in high temporal resolution based on a marker tracking approach (Martrack Leaf).Crossref | GoogleScholarGoogle Scholar |
Milford GFJ, Pocock TO, Riley J, Messem AB (1985) An analysis of leaf growth in sugar beet. Annals of Applied Biology 106, 187–203.
| An analysis of leaf growth in sugar beet.Crossref | GoogleScholarGoogle Scholar |
Miralles DJ, Ferro BC, Slafer GA (2001) Developmental responses to sowing date in wheat, barley and rapeseed. Field Crops Research 71, 211–223.
| Developmental responses to sowing date in wheat, barley and rapeseed.Crossref | GoogleScholarGoogle Scholar |
Nagelmüller S, Kirchgessner N, Yates S, Hiltpold M, Walter A (2016) Leaf length tracker: a novel approach to analyse leaf elongation close to the thermal limit of growth in the field. Journal of Experimental Botany 67, 1897–1906.
| Leaf length tracker: a novel approach to analyse leaf elongation close to the thermal limit of growth in the field.Crossref | GoogleScholarGoogle Scholar |
Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358
| Rhythmic growth explained by coincidence between internal and external cues.Crossref | GoogleScholarGoogle Scholar |
Østrem L, Rapacz M, Larsen A, Dalmannsdottir S, Jørgensen M (2015) Influences of growth cessation and photoacclimation on winter survival of non-native Lolium–Festuca grasses in high-latitude regions. Environmental and Experimental Botany 111, 21–31.
| Influences of growth cessation and photoacclimation on winter survival of non-native Lolium–Festuca grasses in high-latitude regions.Crossref | GoogleScholarGoogle Scholar |
Parent B, Tardieu F (2012) Temperature responses of developmental processes have not been affected by breeding in different ecological areas for 17 crop species. New Phytologist 194, 760–774.
| Temperature responses of developmental processes have not been affected by breeding in different ecological areas for 17 crop species.Crossref | GoogleScholarGoogle Scholar |
Pfeifer J, Mielewczik M, Friedli M, Kirchgessner N, Walter A (2018) Non-destructive measurement of soybean leaf thickness via X-ray computed tomography allows the study of diel leaf growth rhythms in the third dimension. Journal of Plant Research 131, 111–124.
| Non-destructive measurement of soybean leaf thickness via X-ray computed tomography allows the study of diel leaf growth rhythms in the third dimension.Crossref | GoogleScholarGoogle Scholar |
Poiré R, Wiese-Klinkenberg A, Parent B, Mielewczik M, Schurr U, Tardieu F, Walter A (2010) Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects. Journal of Experimental Botany 61, 1751–1759.
| Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects.Crossref | GoogleScholarGoogle Scholar |
Porter JR, Gawith M (1999) Temperatures and the growth and development of wheat: a review. European Journal of Agronomy 10, 23–36.
| Temperatures and the growth and development of wheat: a review.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2014) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 6 May 2017]
Rapacz M (1998) The effects of day and night temperatures during early growth of winter oilseed rape (Brassica napus L. var. oleifera cv. Górczański) seedlings on their morphology and cold acclimation responses. Acta Physiologiae Plantarum 20, 67–72.
| The effects of day and night temperatures during early growth of winter oilseed rape (Brassica napus L. var. oleifera cv. Górczański) seedlings on their morphology and cold acclimation responses.Crossref | GoogleScholarGoogle Scholar |
Rapacz M, Tokarz K, Janowiak F (2001) The initiation of elongation growth during long-term low-temperature stay of spring-type oilseed rape may trigger loss of frost resistance and changes in photosynthetic apparatus. Plant Science 161, 221–230.
| The initiation of elongation growth during long-term low-temperature stay of spring-type oilseed rape may trigger loss of frost resistance and changes in photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |
Richner W, Flisch R, Sinaj S, Charles R (2010) Ableitung der Stickstoffdüngungsnormen von Ackerkulturen. Agrarforschung Schweiz 1, 410–415.
Robeson SM (2002) Increasing growing-season length in Illinois during the 20th century. Climatic Change 52, 219–238.
| Increasing growing-season length in Illinois during the 20th century.Crossref | GoogleScholarGoogle Scholar |
Ruts T, Matsubara S, Wiese‐Klinkenberg A, Walter A (2012) Aberrant temporal growth pattern and morphology of root and shoot caused by a defective circadian clock in Arabidopsis thaliana. The Plant Journal 72, 154–161.
| Aberrant temporal growth pattern and morphology of root and shoot caused by a defective circadian clock in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Sadok W, Naudin P, Boussuge B, Muller B, Welcker C, Tardieu F (2007) Leaf growth rate per unit thermal time follows QTL‐dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions. Plant, Cell & Environment 30, 135–146.
| Leaf growth rate per unit thermal time follows QTL‐dependent daily patterns in hundreds of maize lines under naturally fluctuating conditions.Crossref | GoogleScholarGoogle Scholar |
Sakai A, Larcher W (2012) ‘Frost survival of plants. Responses and adaptation to freezing stress. Ecologies Studies, Vol. 62: Analysis and synthesis.’ (Springer Science & Business Media: Berlin)
Skaggs RH, Baker DG (1985) Fluctuations in the length of the growing season in Minnesota. Climatic Change 7, 403–414.
| Fluctuations in the length of the growing season in Minnesota.Crossref | GoogleScholarGoogle Scholar |
Slafer GA, Savin R (1991) Developmental base temperature in different phenological phases of wheat (Triticum aestivum). Journal of Experimental Botany 42, 1077–1082.
| Developmental base temperature in different phenological phases of wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |
Stefanowska M, Kuras M, Kubacka-Zebalska M, Kacperska A (1999) Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.). Annals of Botany 84, 313–319.
| Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.).Crossref | GoogleScholarGoogle Scholar |
Tardieu F, Granier C, Muller B (1999) Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate? New Phytologist 143, 33–43.
| Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate?Crossref | GoogleScholarGoogle Scholar |
Tian T, Wu L, Henke M, Ali B, Zhou W, Buck-Sorlin G (2017) Modeling allometric relationships in leaves of young rapeseed (Brassica napus L.) grown at different temperature treatments. Frontiers in Plant Science 8, 313
| Modeling allometric relationships in leaves of young rapeseed (Brassica napus L.) grown at different temperature treatments.Crossref | GoogleScholarGoogle Scholar |
Vigil MF, Anderson RL, Beard WE (1997) Base temperature and growing-degree-hour requirements for the emergence of canola. Crop Science 37, 844–849.
| Base temperature and growing-degree-hour requirements for the emergence of canola.Crossref | GoogleScholarGoogle Scholar |
Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 60, 279–304.
| Environmental effects on spatial and temporal patterns of leaf and root growth.Crossref | GoogleScholarGoogle Scholar |
Webb AAR (2003) The physiology of circadian rhythms in plants. New Phytologist 160, 281–303.
| The physiology of circadian rhythms in plants.Crossref | GoogleScholarGoogle Scholar |
Wickham H (2009) ‘ggplot2. Elegant graphics for data analysis.’ (Springer Science & Business Media: New York)
Zhang GQ, Zhang DQ, Tang GX, He Y, Zhou WJ (2006) Plant development from microspore-derived embryos in oilseed rape as affected by chilling, desiccation and cotyledon excision. Biologia Plantarum 50, 180–186.
| Plant development from microspore-derived embryos in oilseed rape as affected by chilling, desiccation and cotyledon excision.Crossref | GoogleScholarGoogle Scholar |
