Seasonal and daily variations in primary and secondary metabolism of three maquis shrubs unveil different adaptive responses to Mediterranean climate

Abstract

Maquis species play a central role in the maintenance of coastal ecosystems thanks to anatomical, physiological and biochemical features evolved to cope with severe stress conditions. Because the seasonal and daily dynamics of physiological and biochemical traits of maquis species are not fully addressed, we performed a field study on three coexisting Mediterranean shrubs (Pistacia lentiscus L. and Phillyrea latifolia L., evergreen schlerophylls, and Cistus incanus L., semi-deciduous) aiming at detecting the main adaptive differences, on a seasonal and daily basis, in primary and secondary metabolism along with the principal climatic determinants. These species differed in their physiological and biochemical responses especially on a seasonal level. In P. latifolia, a great investment in antioxidant phenylpropanoids contributed to maintain high photosynthetic rates throughout the whole growing season. In C. incanus, high carotenoid content associated with chlorophyll (Chl) regulation alleviated oxidative damage during the hot and dry summers and help recover photosynthesis in autumn. In P. lentiscus, high abscisic acid levels allowed a strict control of stomata, while fine Chla/Chlb regulation concurred to avoid photoinhibition in summer. Temperature resulted the most important climatic factor controlling the physiological and biochemical status of these coexisting shrubs and, thus, in determining plant performances in this Mediterranean coastal habitat.

Keywords: Abscisic acid; Mediterranean climate; coastal dune ecosystems; gas exchange; maquis species; photosynthetic pigments; polyphenols; water relations.

Figure 1

Monthly total precipitation (mm), daily average of maximum and minimum air temperature in 2014 and 2015 (a) (arrows indicate the sampling months); year averages of daily global irradiance (W m⁻²) during the days of measurements (b) (data of the Meteorological Station of Ponti di Badia, Grosseto).

Figure 2

Seasonal trends of (a) net photosynthetic rate (P_n) and (b) stomatal conductance (g_s) in C. incanus, P. latifolia and P. lentiscus. Data are means ± SD (n = 32). Letters indicate significant differences (p ≤ 0.05) among species for each season, whereas asterisks indicate significant differences (p ≤ 0.05) among seasons for each species.

Figure 3

Relationship between net photosynthetic rate (P_n) and stomatal conductance (g_s) in C. incanus, P. latifolia and P. lentiscus measured in spring, summer and autumn. Dara are means ± SD (n = 9). The central black line indicates the line of best-fit. The dotted lines either side of the best-fit line indicate 95% confidence intervals of the mean. P and r² values indicate the results of linear regression.

Figure 4

Relationship between midday water potential (Ψ_wMD) and midday stomatal conductance (g_sMD) (a), and between midday water potential (Ψ_wMD) and midday intrinsic water use efficiency (WUEi_MD) (b) in C. incanus, P. latifolia and P. lentiscus in spring, summer and autumn. Dara are means ± SD (n = 3). The lines indicate the best-fit for the three species; p and r² values indicate the results of linear regression.

Figure 5

Diurnal trends of maximal efficiency of maximum photochemical efficiency of PSII (F_v/F_m) and actual efficiency of the PSII (Φ_PSII) measured in spring (a, d), summer (b, e) and autumn (c, f) in C. incanus, P. latifolia and P. lentiscus. Data are means ± SD (n = 8). Letters indicate significant differences (p ≤ 0.05) among hours for each species, whereas asterisks indicate significant differences (p ≤ 0.05) among species for each hour.

Figure 6

Relationship between NPQ, and de-epoxidation state of the DES in C. incanus, P. latifolia and P. lentiscus measured daily in spring, summer and autumn. Dara are means ± SD (n = 36). The central black line indicates the line of best-fit. The dotted lines either side of the best-fit line indicate 95% confidence intervals of the mean; p and r² values indicate the results of linear regression.

Figure 7

Seasonal trends in (a) total carotenoid content (Car_Tot), (b) total chlorophyll content (Chl_Tot), (c) xanthophyll cycle pigments to chlorophyll total ratio (VAZ/Chl_Tot), and (d) chlorophyll a to chlorophyll b ratio (Chla/Chlb) in C. incanus, P. latifolia and P. lentiscus. Data are means ± SD (n = 32). Letters indicate significant differences (p ≤ 0.05) among species for each season, whereas asterisks indicate significant differences (p ≤ 0.05) among seasons for each species.

Figure 8

Relationship between net photosynthetic rate (P_n) and total chlorophyll content (Chl_Tot) in C. incanus, P. latifolia and P. lentiscus in spring, summer and autumn. Dara are means ± SD (n = 3). The lines indicate the best-fit for the three species. P and r² values indicate the results of linear regression.

Figure 9

Seasonal trends in content of (a) total polyphenols (POL_Tot) and (b) total phenylpropanoids (PP_Tot) in C. incanus, P. latifolia and P. lentiscus. Data are means ± SD (n = 32). Different lower-case letters indicate significant differences (p ≤ 0.05) among species for each season, whereas asterisks indicate significant differences (p ≤ 0.05) among seasons for each species.

Figure 10

Seasonal variation in content of (a) ABA and (b) ABA-GE in C. incanus, P. latifolia and P. lentiscus. Data are means ± SD (n = 32). Letters indicate significant differences (P ≤ 0.05) among species for each season, whereas asterisks indicate significant differences (p ≤ 0.05) among seasons for each species.

Figure 11

PCA performed using physiological traits ( P_n, g_s, Ψ_w, Ψ_π, Φ_PSII, NPQ and Fv/F_m,) and biochemical traits (PP_Tot, Car_Tot, Chl_Tot Chla/Chlb and ABA) in spring (a) summer (b) and autumn (c) for the considered species. In the parentheses it is shown the percentage of total variation explained by each PC axis and the relative eigenvalues.