Abstract
Germplasm degeneration causes serious problems for the Chinese Pyropia yezoensis industry. A subtidal P. yezoensis strain was introduced into aquaculture. The desiccation tolerance of this strain is compared by using “periodically drying” and “never drying” culture protocols. The thalli with periodical drying tolerated ~70% relative water loss (RWL) while those cultured without “drying” endured ≤50% RWL. Pigment contents were higher in the thalli with periodical drying than those farmed without drying. Chlorophyll a and carotenoid levels from both systems decreased significantly at RWL = 20%, were steady at RWL = 20–50%, and decreased at RWL = 60%. Phycoerythrin, phycocyanin, and soluble proteins (SPs) contents from the periodically drying system decreased significantly at RWL = 20%, while those from the never drying system remained steady at RWL = 0–50%. For (phycoerythrin + phycocyanin): SPs from either system increased during dehydration and peaked at the critical point of desiccation tolerance. Superoxide dismutase (SOD), catalase, and peroxidase activities peaked at RWL = 40–50% in the never drying system and 60–70% in the periodically drying system. The results suggested that SOD, catalase, and peroxidase played important roles in desiccation tolerance of this strain. Phycoerythrin, phycocyanin, and carotenoid could dissipate the excess energy as heat or directly scavenge reactive oxygen species. Thus, no significant malondialdehyde was accumulated during dehydration. In conclusion, with and without periodically drying during P. yezoensis farming affected the desiccation tolerance, pigments and SP contents, and antioxidase activities. The subtidal strain seemed to prefer the never drying culture protocol in terms of SPs content and SOD, CAT, and POD activities.
Similar content being viewed by others
References
Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584
Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum: a contribution to the study of drought tolerance at the molecular level. Plant Physiol 127:1346–1353
Burritt DJ, Larkindale J, Hurd K (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838
Cao Y, Wang WJ, Liang ZR, Liu FL, Sun XT, Yao HQ, Li XL, Wang FJ (2016) Genetic and nutrient analysis of new Pyropia yezoensis strain “Huangyou No. 1”. Guangxi Sci 23(2):131–137 (in Chinese with English abstract)
Chen CS, Weng L, Wang L, Ji DH, Xie CT, Xu Y (2007) Influence of desiccation and cold preservation on the survival and growth of Porphyra haitanensis and unwanted alga. Acta Oceanol Sin 29(2):131–136 (in Chinese with English abstract)
Collén J, Guisle-Marsollier I, Léger JJ, Boyen C (2007) Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytol 176:45–55
Contreras-Porcia L, Thomas D, Flores V, Correa JA (2011) Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J Exp Bot 62:1815–1829
Contreras-Porcia L, López-Cristoffanini C, Lovazzano C, Flores-Molina MR, Thomas D, Núñez A, Fierro C, Guajardo E, Correa JA, Kube M, Reinhardt R (2013) Differential gene expression in Pyropia columbina (Bangiales, Rhodophyta) under natural hydration and desiccation conditions. Lat Am J Aquat Res 41:933–958
Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prásil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17
Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211
Druehl LD, Green JM (1982) Vertical distribution of intertidal seaweeds as related to patterns of submersion and emersion. Mar Ecol Prog Ser 9:163–170
Gao K, Aruga Y (1987) Preliminary studies on the photosynthesis and respiration of Porphyra yezoensis under emersed conditions. J Tokyo Univ Fish 47:51–65
Gao S, Wang GC (2012) The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). J Exp Bot 63:4349–4358
Green LA, Neefus CD (2015) Effects of temperature, light level, photoperiod, and ammonium concentration on Pyropia leucosticta (Bangiales, Rhodophyta) from the Northwest Atlantic. J Appl Phycol 27:1253–1261
Guajardo E, Correa JA, Contreras-Porcia L (2016) Role of abscisic acid (ABA) in activating antioxidant tolerance response to desiccation stress in intertidal seaweed species. Planta 243:767–781
Hader D, Lebert M, Sinha RP, Barbieri ES, Helbling EW (2002) Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem Photobiol Sci 1:809–814
Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a Bzip transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230
Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45:771–787
Jiang H, Gao K, Helbling EW (2008) UV-absorbing compounds in Porphyra haitanensis (Rhodphyta) with special reference to effects of desiccation. J Appl Phycol 20:387–395
Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24
Li XL, Wang WJ, Liang ZR, Liu FL, Sun XT, Cao Y, Yao HQ, Wang FJ (2017) Antioxidant physiological characteristics of wild Pyropia yezoensis under desiccation stress. Mar Fish Res in press. (in Chinese with English abstract)
Lin AP, Wang GC, Yang F, Pan GH (2009) Photosynthetic parameters of sexually different parts of Porphyra katadai var. hemiphylla (Bangiales, Rhodophyta) during dehydration and rehydration. Planta 229:803–810
Liu YC (2009) Mechanism for differential desiccation tolerance in Porphyra species. Thesis, Northeastern University, Boston, USA
Niwa K, Iida S, Kato A, Kawai H, Kikuchi N, Kobiyama A, Aruga Y (2009) Genetic diversity and introgression in two cultivated species (Porphyra yezoensis and Porphyra tenera) and closely related wild species of Porphyra (Bangiales, Rhodophyta). J Phycol 45:493–502
Oh S, Shin M, Lee K, Choe E (2013) Effects of water activity on pigments in dried laver (Porphyra) during storage. Food Sci Biotechnol 22:1523–1529
Oliver MJ, Velten J, Mishler B (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156
Read S, Northcote D (1981) Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal Biochem 116:53–64
Romay C, González R, Ledón N, Remirez D, Rimbau V (2003) C-phycocyanin, a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4:207–216
Sampath-Wiley P, Neefus CD (2007) An improved method for estimating R-phycoerythrin and R-phycocyanin contents from crude aqueous extracts of Porphyra (Bangiales, Rhodophyta). J Appl Phycol 19:123–129
Shen D, Wu M (1995) Chromosomal and mutagenic study of the marine macroalga, Gracilaria enuistipitata. J Appl Phycol 7:26–30
Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi HG, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151
Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270
Tandeau de Marsac N (2003) Phycobiliproteins and phycobilisomes, the early observation. Photobiol Res 76:197–205
Vranová E, Inzé D, Van Breusegen F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236
Wang WJ, Zhu JY, Xu P, Xu JR, Lin XZ, Huang CK, Song W, Peng G, Wang GC (2008) Characterization of the life history of Bangia fuscopurpurea (Bangiaceae, Rhodophyta) in connection with its artificial cultivation in China. Aquaculture 278:101–109
Wang WJ, Wang FJ, Zhu JY, Sun XT, Yao CY, Xu P (2011) Freezing tolerance of Porphyra yezoensis (Bangiales, Rhodophyta) gametophyte assessed by chlorophyll fluorescence. J Appl Phycol 23:1017–1022
Wang WJ, Sun XT, Liu FL, Liang RZ, Zhang JH, Wang FJ (2016) Effect of abiotic stress on the gameophyte of Pyropia katadae var. hemiphylla (Bangiales, Rhodophyta). J Appl Phycol 28:469–479
Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014) Effect of irradiance and temperature on the photosynthesis of a cultivated red alga, Pyropia tenera (= Porphyra tenera), at the southern limit of distribution in Japan. Phycol Res 62:187–196
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Xie J, Xu Y, Ji D, Chen C, Xie C (2014) Physiological response of the antioxidant system in Pyropia haitanensis to desiccation stress. J Fish Sci China 21(2):405–412 (in Chinese with English abstract)
Xu Y, Gao S, Yang Y, Huang M, Cheng L, Wei Q, Fei Z, Hong B (2013) Transcriptome sequencing and whole genome expression profiling of chrysanthemum under dehydration stress. BMC Genomics 14:662
Zeng Y, Kermode AR (2004) A gymnosperm ABI3 gene functions in a severe abscisic acid-insensitive mutant of Arabidopsis (abi3-6) to restore the wild-type phenotype and demonstrates a strong synergistic effect with sugar in the inhibition of post-germinative growth. Plant Mol Biol 56:731–746
Zheng BF, Li Y (2009) Rhodophyta No. 1 Porphyridiales, Erythropeltidales, Goniotrichales, Bangiales. In: Flora algarum marinarum sinicarum. Science Publisher, Beijing, pp 56–105
Zhong ZH, Wang WJ, Sun XT, Liu FL, Liang ZR, Wang FJ, Chen WZ (2016) Developmental and physiological properties of Porphyra dentata (Bangiales, Rhodophyta) conchocelis in culture. J Appl Phycol 28:3435–3445
Zhou W, He L, Yang F, Lin A, Zhang B, Niu J, Wang G (2014) Pyropia yezoensis can utilize CO2 in the air during moderate dehydration. Chin J Oceanol Limnol 32:358–364
Zou D, Gao K (2002) Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. Eur J Phycol 37:587–592
Zou D, Gao K (2004) Exogenous carbon acquisition of photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta) under emersed state. Prog Nat Sci 14(2):138–144
Acknowledgements
This work was supported by the Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (No. 2015A02), the Primary Research & Development Plan of Shandong Province (2016GSF115038), and the Science and Technology Plan of Changdao (2016-2018).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, Xl., Wang, Wj., Liu, Fl. et al. Periodical drying or no drying during aquaculture affects the desiccation tolerance of a sublittoral Pyropia yezoensis strain. J Appl Phycol 30, 697–705 (2018). https://doi.org/10.1007/s10811-017-1227-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-017-1227-y