Desiccation Stress Tolerance in Porphyra and Pyropia Species: A Latitudinal Analysis along the Chilean Coast

Abstract

One of the most important factors regulating the distribution and abundance of seaweeds is desiccation, triggered mainly by tidal changes and climatic variation. Porphyra and Pyropia species have evolved multiple strategies to tolerate desiccation stress; however, how these tolerance strategies differ in these species inhabiting different latitudes is still unknown. In this context, we analyzed, in situ, the physiological responses of these species (collected from 18° S to 41° S along the Chilean coast) to desiccation stress using biochemical and molecular analyses. The hyper-arid terrestrial climate of northern Chile, with high evaporation and lack of constant rain determines a very steep increase in desiccation stress in the upper intertidal during low tide for these species. Accordingly, the results showed that, in comparison with the southernmost populations, the Porphyra/Pyropia species from the north zone of Chile (18°-30° S) exhibited higher contents of lipoperoxide and carbonyls (1.6-1.9 fold) together with higher enzymatic activities, including ascorbate peroxidase, catalase, peroxiredoxin, and thioredoxin (2-3-fold). In addition, a substantial expression of cat, prx, and trx transcripts during desiccation was demonstrated, mainly in the northernmost populations. These results provide evidence of (i) significant activation of antioxidant enzymes and transcripts (principally cat and prx); (ii) participation of phenolic antioxidant compounds as a highly plastic physiological strategy to cope with desiccation; and (iii) the activation of the tolerance responses was affected by species latitudinal distribution. Thus, for the first time, this study integrated the biochemical and genetic responses of diverse Porphyra/Pyropia species to better understand their physiological dynamics of tolerance over a wide latitudinal range.

Keywords: Laver; Luche; Nori; antioxidants; desiccation stress; latitudinal distribution; ocean warming; oxidative stress; reactive oxygen species; red seaweeds.

Figure 1

Specific activity of PDH (pyruvate dehydrogenase) during natural hydration (H) and desiccation (D) stress in the Porphyra and Pyropia species evaluated in this study. Values are the mean ± SD of three replicates. ARI, Arica; ANT, Antofagasta; GUA, Guanaquerillos; LSV, Los Vilos; MAI, Maitencillo; PDT, Punta de Tralca; PIC, Pichilemu; COL, Coliumo; CAL, Calfuco; NIE, Niebla; CAR, Carelmapu; and ANC, Ancud (see Table 1 and Figure 6 for in-depth information).

Figure 2

Specific activity of (A) AP (ascorbate peroxidase) and (B) CAT (catalase) during in situ hydration (H) and desiccation (D) stress in the Porphyra and Pyropia species evaluated in this study. Values are the mean ± SD of three replicates. ARI, Arica; ANT, Antofagasta; GUA, Guanaquerillos; LSV, Los Vilos; MAI, Maitencillo; PDT, Punta de Tralca; PIC, Pichilemu; COL, Coliumo; CAL, Calfuco; NIE, Niebla; CAR, Carelmapu; and ANC, Ancud (see Table 1 and Figure 6 for in-depth information).

Figure 3

Specific activity of (A) PRX (peroxiredoxin) and (B) TRX (thioredoxin) during in situ hydration (H) and desiccation (D) stress in the Porphyra and Pyropia species evaluated in this study. Values are the mean ± SD of three replicates. ARI, Arica; ANT, Antofagasta; GUA, Guanaquerillos; LSV, Los Vilos; MAI, Maitencillo; PDT, Punta de Tralca; PIC, Pichilemu; COL, Coliumo; CAL, Calfuco; NIE, Niebla; CAR, Carelmapu; and ANC, Ancud (see Table 1 and Figure 6 for in-depth information).

Figure 4

(A) Lipid peroxidation, (B) protein oxidation, and (C) phenolic compound concentrations during in situ hydration (H) and desiccation (D) stress in the Porphyra and Pyropia species evaluated in this study. Values are the mean ± SD of three replicates. ARI, Arica; ANT, Antofagasta; GUA, Guanaquerillos; LSV, Los Vilos; MAI, Maitencillo; PDT, Punta de Tralca; PIC, Pichilemu; COL, Coliumo; CAL, Calfuco; NIE, Niebla; CAR, Carelmapu; and ANC, Ancud (see Table 1 and Figure 6 for in-depth information).

Figure 5

Relative expression level of (A) cat, (B) prx, and (C) trx transcripts during hydration (H), desiccation (D), and rehydration (RH) cycle in Porphyra and Pyropia species (see Table 1 and Figure 6 for details). Values are the mean ± SD of three replicates. The letters above the bar plots indicate the results of Tukey’s tests; means with the same letter are not significantly different at p ≥ 0.05. The colors of the histograms correspond to the sites evaluated.

Figure 6

Sampling sites along the Chilean coast of the Porphyra and Pyropia species studied in this work.