Acclimation of Bryophytes to Sun Conditions, in Comparison to Shade Conditions, Is Influenced by Both Photosynthetic and Ultraviolet Radiations

Abstract

We studied the acclimation modalities of bryophytes to sun and shade under ambient or close-to-ambient conditions, measuring variables usually influenced by photosynthetically active (PAR) and ultraviolet (UV) radiations. Our aim was to elucidate to what extent the responses to changing radiations were influenced by PAR and UV wavelengths. For this aim, we used three taxonomically and structurally different species: the thalloid liverwort Marchantia polymorpha subsp. polymorpha, the leafy liverwort Jungermannia exsertifolia subsp. cordifolia, and the moss Fontinalis antipyretica. In the field, liverworts were more radiation-responsive than the moss, and the thalloid liverwort was more responsive than the leafy liverwort. Sun plants of M. polymorpha showed, in comparison to shade plants, higher sclerophylly, lower Chl a + b contents, higher Chl a/b ratios, higher (antheraxanthin + zeaxanthin)/(violaxanthin + antheraxanthin + zeaxanthin) ratios (xanthophyll index), lower F _v/F _m values, higher contents of methanol-soluble vacuolar UV-absorbing compounds (soluble UVACs), higher values of the ratio between the contents of methanol-insoluble cell wall-bound UVACs (insoluble UVACs) and soluble UVACs, higher contents of soluble luteolin and apigenin derivatives and riccionidin A, and higher contents of insoluble p-coumaric and ferulic acids. Overall, these responses reduced light absorption, alleviated overexcitation, increased photoprotection through non-photochemical energy dissipation, increased UV protection through UV screening and antioxidant capacity, and denoted photoinhibition. J. exsertifolia showed moderate differences between sun and shade plants, while responses of F. antipyretica were rather diffuse. The increase in the xanthophyll index was the most consistent response to sun conditions, occurring in the three species studied. The responses of soluble UVACs were generally clearer than those of insoluble UVACs, probably because insoluble UVACs are relatively immobilized in the cell wall. These modalities of radiation acclimation were reliably summarized by principal components analysis. Using the most radiation-responsive species in the field (M. polymorpha), we found, under close-to-ambient greenhouse conditions, that sclerophylly and Chl a + b content were only influenced by PAR, F _v/F _m, and luteolin and apigenin derivatives were only determined by UV, and xanthophyll index was influenced by both radiation types. Thus, responses of bryophytes to radiation can be better interpreted considering the influence of both PAR and UV radiation.

Keywords: Marchantia; acclimation; bryophytes; chlorophyll; flavonoids; sclerophylly; ultraviolet radiation; xanthophylls.

Figure 1

(Top) Representative spectral irradiance (280–700 nm) measured around midday on sunny days under sun and shade conditions in a typical sampling site. (Bottom) Spectral irradiance (280–700 nm) received by the thalloid liverwort Marchantia polymorpha subsp. polymorpha under the three radiation regimes imposed in the greenhouse experiment: P (PAR alone), P-shaded, and PAB (PAR + UV-A + UV-B).

Figure 2

Comparison (mean ± SE, n = 3) of different variables measured in sun and shade samples of Marchantia polymorpha subsp. polymorpha. SUVAC and IUVAC, total contents of UV-absorbing compounds from the soluble and insoluble fractions, respectively, in terms of the area under the absorbance curve in the interval 280–400 nm (AUC_280–400) per DM unit. SI, sclerophylly index. Significance levels for statistical analysis are shown: ^***p < 0.001; ^**p < 0.01; ^*p < 0.05; ns, non-significant.

Figure 3

Comparison (mean ± SE, n = 3) of different variables measured in sun and shade samples of Jungermannia exsertifolia subsp. cordifolia. SUVAC and IUVAC, total contents of UV-absorbing compounds from the soluble and insoluble fractions, respectively, in terms of the area under the absorbance curve in the interval 280–400 nm (AUC_280–400) per DM unit. SI, sclerophylly index. Significance levels for statistical analysis are shown: ^**p < 0.01; ^*p < 0.05; ns, non-significant.

Figure 4

Comparison (mean ± SE, n = 3) of different variables measured in sun and shade samples of Fontinalis antipyretica. SUVAC and IUVAC, total contents of UV-absorbing compounds from the soluble and insoluble fractions, respectively, in terms of the area under the absorbance curve in the interval 280–400 nm (AUC_280–400) per DM unit. SI, sclerophylly index. Significance levels for statistical analysis are shown: ^*p < 0.05; ns, non-significant.

Figure 5

Ordination, through principal components analysis (PCA), of the sun (yellow) and shade (blue) samples of the three species studied: Marchantia polymorpha subsp. polymorpha (diamonds), Jungermannia exsertifolia subsp. cordifolia (triangles), and Fontinalis antipyretica (circles). SUVAC and IUVAC, total contents of UV-absorbing compounds from the soluble and insoluble fractions, respectively. SI, sclerophylly index. Significant loading factors for the positive and negative parts of each axis, together with their corresponding significance levels, are shown. ^***p < 0.001; ^*p < 0.05. Axis I is the horizontal one, and axis II is the vertical one. Each tick mark on axes I and II represents 1 U.

Figure 6

Variables which showed, in samples of Marchantia polymorpha subsp. polymorpha grown in the greenhouse experiment, significant differences between PAB and P treatments (effect of UV radiation, left column), or between P and P-shaded treatments (effect of PAR level, right column). P, PAR alone. P-shaded, reduced PAR using a shade cloth (see Figure 1, bottom). PAB, PAR + UV-A + UV-B. SI, sclerophylly index. All the results are expressed in relative units, taking the P treatment as the unit value. For each variable, means ± SE (n = 3), together with significance levels for statistical analysis, are shown: ^***p < 0.001; ^**p < 0.01; ^*p < 0.05; ns, non-significant.