Leaf Turgor Loss Does Not Coincide With Cell Plasmolysis in Drought-Tolerant Chaparral Species

Abstract

The water potential at which leaf cells lose turgor (Ψ_TLP) is a useful predictor of whole-plant drought tolerance and biome wetness. However, many plants can achieve water potential values below Ψ_TLP and recover, raising questions about the physiological processes that occur below Ψ_TLP. We established a controlled greenhouse experiment to induce turgor loss on six shrub species from a Mediterranean-type ecosystem in Southern California and characterised physiological and leaf-structural adjustments to Ψ_TLP. We documented seasonal adjustments in Ψ_TLP, both with and without applied drought. Stomatal closure always occurred below Ψ_TLP, and the margin between the two phenomena increased with lower Ψ_TLP. Drought tolerance was strongly correlated with heat tolerance. Most histological responses to Ψ_TLP involved shrinkage of both spongy mesophyll cells and intercellular air spaces, leading to reduced leaf thickness, but not plasmolysis. Overall, our results indicate a propensity to reach Ψ values far below Ψ_TLP and maintain function for extended periods of time in Southern California shrubs. Whereas species in many ecosystems fall below Ψ_TLP for brief periods of time, the erratic nature of precipitation patterns makes Southern California an outlier in the range of operational plant water potentials.

Keywords: chaparral; drought; heat; histology; thermal tolerance; turgor loss point.

Figure 1

Difference between minimum Ψ _leaf at the end of the dry season (September 2021) and Ψ _TLP measured at the same time. Actual Ψ _TLP is shown in numbers above the x‐axis. Symbols indicate the Ψ _leaf − Ψ _TLP. Negative values indicate Ψ _leaf was lower (more negative) than the Ψ _TLP. Error bars show SE (n = 5). Measurements were taken at the Santa Margarita Ecological Reserve on five individuals of each species.

Figure 2

Turgor loss point (Ψ _TLP) as measured in March and July 2022. The value in March shows the average of all plants together. The values in July distinguish between well‐watered (blue) and drought‐stressed (red) plants. Average ± SE are shown. Asterisks indicate significant species differences in July.

Figure 3

The relationship between turgor loss point (Ψ _TLP) and gs90. Blue symbols indicate Ψ _TLP in well‐watered plants, and red symbols are drought‐stressed plants. The light‐grey line indicates a 1:1 line, showing a hypothetical simultaneous Ψ _TLP and gs90. The black line shows a linear regression. Abbreviations: Hear: H. arbutifolia, Qube: Q. berberidifolia, Mala: M. laurina, Ceto: C. tomentosus, Same: S. mellifera, Saap: S. apiana. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4

Correlations between physiological parameters. Turgor loss point versus LMA (a), WUE (b) and T ₅₀ (c); T ₅₀ versus LMA (d) and WUE (e). All data was collected at the end of the experiment, in July 2022. Each point represents one individual (n = 6 for 6 different species, with drought and well‐watered plants all shown). R values indicate the correlation coefficient. A line and correlation coefficient shown indicate a significant correlation between the two variables.

Figure 5

Light microscopy images from C. tomentosus and S. apiana (cross‐section). Images are taken at 10× magnification with a Leica microscope and camera using AmScope imaging software. Red scale bars indicate 100 μm. Red arrows indicate partial plasmolysis of the epidermal cell. Blue arrows show the parameters measured: LT = leaf thickness, SM = spongy mesophyll thickness. Upper images show drought‐stressed leaves, and lower images show well‐watered leaves. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 6

Histological parameters in well‐watered (blue) and drought‐stressed (red) plants of the six species. Boxes show the 95% quantiles. An average of evergreen (C. tomentosus, H. arbutifolia, M. laurina and Q. berberidifolia) and drought‐deciduous species (S. apiana and S. mellifera) is given in the right panel for every parameter. Red colours indicate drought‐stressed, and blue colours well‐watered plants. Most parameters are shown as % of leaf thickness. Asterisks indicate a significant difference between well‐watered and dry treatments (n = 3). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 7

Correlations between histological parameters and physiological traits. Cuticle (a–c), epidermis (d–f), palisade (g–i) and spongy (j–l) mesophyll thickness are expressed in % of leaf thickness and presented in relation to gas exchange rates (a, d, g, j), leaf mass per area (LMA; b, e, h, k) and leaf sugar concentrations (c, f, i, l). Different variants of gas exchange were shown, depending on the statistical significance of the relationship. A_predrought indicates photosynthesis rates before the drought treatment started (March 2022). E and A indicate transpiration and photosynthesis, respectively, at the end of the treatment period (July 2022). Each point represents one individual (n = 6 for 6 different species, with drought and well‐watered plants all shown). Data come from measurements taken at the end of the experiment, in July 2022, unless stated differently (‘_predrought’ suffix, April 2022). Lines and correlation coefficients (r values) indicate significant correlations between two variables.