Daily fluctuations in leaf temperature modulate the development of a foliar pathogen
Introduction
Most organisms grow and evolve in fluctuating environments (Du and Ji, 2006). This is particularly true regarding temperature, a factor that affects many, if not all, physiological processes involved in growth and development (Angilletta, 2009). Temperature fluctuates at various time scales, from minute to years, with periodicity over daily and yearly periods, and each time scale can matter for different physiological processes from thermal tolerance (small time scales) to diapause/quiescence strategies (long time scales) (Dillon et al., 2016). The exchange of energy (radiation, convection, conduction, latent heat) between an organism and its environment generates temperature deviations between the body of organisms and their surrounding air. In ectotherms, the body temperature, subjected to fluctuating solar radiation and wind, and to night sky radiation cooling, is expected to fluctuate more intensively and rapidly than air temperature (Gates, 1980). This paradigm also applies to plant surfaces, which generate a particular thermal environment for the large variety of organisms living on them, from phytophagous arthropods to bacteria and fungal pathogens.
Leaf dwelling organisms experience variations in the temperature of the leaf surface rather than in ambient air (Pincebourde and Woods, 2012; Pincebourde et al., 2021; Scherm and van Bruggen, 1993). Temperature heterogeneity in space and time over leaf surface can depart largely from ambient air, with deviation of up to 20 °C between a specific leaf area and ambient air (Saudreau et al.. 2017). The potential effects of large thermal amplitude on biological processes within the leaf envelope have been considered in studies on the effect of climate variations on arthropod development (Bradshaw et al., 2000; Kingsolver, 1979; Pincebourde and Casas, 2006; Potter et al., 2009; Pincebourde and Suppo, 2016). The influence of the ‘phylloclimate’ (the microclimatic conditions occurring in the phyllosphere; Chelle, 2005) is presumed to be high on the whole leaf microbiota (Pincebourde and Woods, 2012; Vacher et al., 2016). Many studies focused on the impact of (constant) temperature on plant disease cycles (incubation, latent period, senescence, etc.), both by experimental and modeling approaches (de Wolf and Isard, 2007), but the impact of the fluctuation of leaf temperature on the development of leaf fungal pathogens has never been studied, except partly by Bonde et al. (2012). Some studies focused on entire living plants or detached leaves (e.g. Scherm and van Bruggen, 1994a; Xu, 1996; Shakya et al., 2015) but were based on air temperature fluctuations, while some others were carried out on artificial media instead of leaf (e.g. Zhan and McDonald, 2011; Boixel et al., 2019). This last experimental approach has two main drawbacks: (i) a Petri dish or wells of a microplate does not have the same energy budget as a living leaf; (ii) only the direct effect of temperature on the fungus can be observed, while the complex interrelationship between environmental temperature, leaf temperature, and the foliar and fungal responses are ignored. Therefore, the use of artificial media limits our ability to apply growth predictions to more natural situations.
Mean temperature can be an uninformative, even misleading, descriptor of a fluctuating thermal environment (Kingsolver et al., 2004). Thermal fluctuations likely matter for the growth of fungal pathogens. Scherm and van Bruggen (1994b) were the first to demonstrate theoretically that the difference between growth of plant fungal pathogens at constant versus fluctuating temperatures is maximized when the mean temperature is close to one of the three cardinal temperatures (minimal, optimal and maximal temperatures) and/or when the temperature range over which the growth response is approximately linear is narrow. As an example, the use of daily mean temperature to predict the incubation period (for plant pathologists, the time needed for the first symptoms to appear) and the latent period (the ‘generation time’, i.e. the duration between inoculation and the appearance of fruiting bodies releasing contaminating spores) of a fungal pathogen under field conditions may result in errors when the underlying rate function is non-linear (Xu, 1996). A higher resolution in temperatures is therefore required, and several studies showed that the hourly time step increased the accuracy of predictions (Narouei-Khandan et al., 2020; Salotti and Rossi, 2021). The model developed by Narouei-Khandan et al. (2020) to simulate effects of daily amplitudes on the development of late blight highlighted a significant interaction between average air temperature and amplitude in their effects on the area under the disease progress curve (AUDPC) as predicted from growth chamber data on a single infection cycle. Greater effects of amplitudes were observed at the extreme temperatures (including the optimal temperature), and no amplitude effect at the inflection point of the optimal temperature curve. The importance of daily temperature fluctuations was also demonstrated by Salotti and Rossi (2021) for the development of Ascochyta blight on chickpeas. Environmental sampling rate, such as the frequency of temperature recording (duration of time step), relative to the frequency of leaf temperature changes, is therefore crucial when predicting organism fitness, yet few studies have quantified its importance.
The objective of this study was to assess the relevance of using leaf temperature rather than air temperature as climatic driver by (i) comparing daily amplitudes of leaf and air temperatures in field conditions, and (ii) comparing the in planta development of a foliar fungal pathogen under two leaf temperature regimes of equal mean but differing in their daily leaf thermal amplitude (DLTA). As a case study, we used the fungus Zymoseptoria tritici (formerly Mycosphaerella graminicola), the causal agent of Septoria tritici blotch disease on wheat. Present wherever wheat is grown and developing throughout the wheat growing season (Suffert and Sache, 2011), the pathogen is exposed to a wide range of mean and amplitude temperatures across its geographical distribution (Suffert et al., 2015). Finally, we used a simple mathematical model based on a non-linear relationship of fungal performance to temperature (see Supplementary Materials) to provide additional support for discussing on the importance of daily temperature amplitude relative to both the shape of the nonlinear growth curve and the frequency of temperature recordings.
Section snippets
Study site
Field experiments were conducted on a winter wheat (Triticum aestivum, cv Tremie) plot established on a deep silt loam soil, at INRAE Thiverval-Grignon, France (48° 50′ 43" N, 1° 56′ 45" E). The crop was conducted as a conventional crop with high sowing density (250 grains.m−2; sowing date 25 October 2011) and nitrogen supply (210 kg.ha−1). No irrigation was supplied.
Temperature measurements
During the development of the flag leaf (from 14 May 2012 to 11 July 2012), the environmental temperature was estimated from the
Comparison between leaf and air temperatures in field conditions
The daily mean leaf temperature was very similar to (P = 0.88), and correlated to the daily mean air temperature (R² = 0.98; Fig. 3a). In 90% of cases, the difference between the two mean temperatures was below 0.7 °C. In contrast, the daily amplitude was higher for leaf temperature than for air temperature (Fig. 3b; P < 0.001). On average, the daily amplitude was 5.8 °C higher for the leaf temperature (14.1 ± 3.8 °C) than for the air temperature (8.3 ± 2.9 °C). We refined these differences in
Discussion
We established in field conditions that the daily amplitude can be highly dependent on the type of temperature even if the average remains the same: air commonly measured by a weather station vs leaf, i.e., in more general terms ‘environmental’ vs ‘body’ temperature. Concretely, the temperature range of a wheat flag leaf is greater than that of air temperature. This can be explained by two mechanisms. During the day, solar radiation hits the leaf, increasing its surface temperature relative to
Conclusion
Incorporating microclimatic conditions (‘phylloclimate’) and the thermal reaction norm of plant pathogens when studying their interaction with plant hosts is a convincing way to develop future disease management in the frame of agroecology (Nicholls and Altieri, 2007). Our study suggested the importance of considering daily leaf temperature amplitudes – and not only the average leaf temperature or daily air temperature amplitudes – when investigating the development of foliar fungal pathogens.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Fabrice Duhamel for technical assistance on experiments. This study was funded by INRAE (‘Plant Health and Environment’ and ‘Environment and Agronomy’ Divisions), ARVALIS – Institut du Végétal (CIFRE PhD fellowship), and the French National Research Agency (grant of the ‘Investissements d'Avenir’ programme; SEPTOVAR project; LabEx BASC; ANR-11-LABX-0034). Finally, we are very grateful for the insightful and helpful comments of the anonymous reviewers.
References (57)
Estimating and comparing thermal performance curves
J. Therm. Biol.
(2006)- et al.
MiteSim – a simulation model of the banks grass mite (Acari: Tetranychidae) and the predatory mite, neoseiulus fallacis (Acari: Phytoseiidae) on maize: model development and validation
Ecol. Model.
(1991) - et al.
Advances in monitoring and modelling climate at ecologically relevant scales
Adv. Ecol. Res.
(2018) - et al.
Using biological insight and pragmatism when thinking about pseudoreplication
Trends Ecol. Evol.
(2018) - et al.
Asynchronous development of Zymoseptoria tritici infection in wheat
Fungal Genet. Biol.
(2021) - et al.
Jensen's inequality predicts effects of environmental variation
Trends Ecol. Evol.
(1999) - et al.
Sensitivity of simulated dew duration to meteorological variations in different climatic regions of California
Agric. For. Meteorol.
(1993) - et al.
A comparison of different thermal performance functions describing temperature-dependent development rates
J. Therm. Biol.
(2010) Thermal Adaptation - A Theoretical and Empirical Synthesis
(2009)Differential effect of light intensity on the infection of wheat by Septoria tritici Desm. under controlled environmental conditions
Physiol. Plant Pathol.
(1971)