Abstract
Haberlea rhodopensis belongs to the small group of resurrection plants having the unique ability to survive desiccation to air dry state retaining most of its chlorophyll content and then resume normal function upon rehydration. It prefers the shady valleys and northward facing slopes of limestone ridges in mountain zones with high average humidity. Nevertheless, it can be found rarely on rocks directly exposed to the sunlight, without the coverage of the canopy. In the present study, we follow the alterations in the subcellular organization of mesophyll cells and sugar metabolism upon desiccation of shade and sun H. rhodopensis plants. Composition and content of soluble carbohydrates during desiccation and rehydration were different in plants grown below the trees or on the sunny rocks. Sucrose, however, was dominating in both ecotypes. The amount of starch grains in chloroplasts was inversely related to that of sugars. Concomitantly with these changes, the number of vacuoles was multiplied in the cells. This can be explained by the development of small (secondary) vacuoles peripherally in the cytoplasm, rather than by the fragmentation of the single vacuole, proposed earlier in the literature. Accordingly, the centripetal movement of chloroplasts and other organelles may be a result of the dynamic changes in the vacuolar system. Upon rehydration, the inner vacuoles enlarged and the organelles returned to their normal position.
Similar content being viewed by others
References
Albini FM, Murelli C, Finzi PV, Ferrarotti M, Cantoni B, Puliga S, Vazzana C (1999) Galactinol in the leaves of the resurrection plant Boea hygroscopica. Phytochemistry 51:499–505
Allison SD, Chang B, Randolph TW, Carpenter JF (1999) Hydrogen bonding between sugar and protein is responsible for inhibition of dehydration-induced protein unfolding. Arch Biochem Biophys 365:289–298
Alpert P (2006) The limits and frontiers of desiccation tolerant life. Integr Comp Biol 45:685–695
Austin JR, Frost E, Vidi P-E, Kessler F, Staehelin LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703
Barrieu F, Marty-Mazars D, Thomas D, Chaumont F, Charbonnier M, Marty F (1999) Desiccation and osmotic stress increase the abundance of mRNA of the tonoplast aquaporin BobTIP26-1 in cauliflower cells. Planta 209:77–86
Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1991a) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1:355–359
Bianchi G, Murelli C, Bochicchio A, Vazzana C (1991b) Changes of low-molecular weight substances in Boea hygroscopica in response to desiccation and rehydration. Phytochemistry 30:461–466
Charuvi D, Nevo R, Shimoni E, Naveh L, Zia A, Adam Z, Farrant JM, Kirchhoffd H, Reich Z (2015) Photoprotection conferred by changes in photosynthetic protein levels and organization during dehydration of a homoiochlorophyllous resurrection plant. Plant Physiol 167:1554–1565
Crowe JH, Carptenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103
Dalla Vecchia F, Asmar TE, Calamassi R, Rascio N, Vazzana C (1998) Morphological and ultrastructural aspects of dehydration and rehydration in leaves of Sporobolus stapfianus. Plant Growth Regul 24:219–228
Daskalova E, Dontcheva S, Yahoubian G, Minkov I, Toneva V (2011) A strategy for conservation and investigation of the protected resurrection plant Haberlea rhodopensis Friv. BioRisk 6:41–60
Farrant JM (2000) A comparison of mechanisms of desiccation-tolerance among three angiosperm resurrection plant species. Plant Ecol 151:29–39
Gaff DF (1971) Desiccation-tolerant flowering plants in southern Africa. Science 174:1033–1034
Gaff DF, Zee SY, O’Brien TP (1976) The fine structure of dehydrated and reviving leaves of Borya nitida Labill.—a desiccation-tolerant plant. Aust J Bot 24:225–236
Gechev TS, Benina M, Obata T, Tohge T, Sujeeth N, Minkov I, Hille J, Temanni M-R, Marriott AS, Bergström E, Thomas-Oates J, Antonio C, Mueller-Roeber B, Schippers JHM, Fernie AR, Toneva V (2013) Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell Mol Life Sci 70:689–709
Georgieva K, Maslenkova L (2006) Thermostability and photostabitity of PSII in leaves of resurrection plant Haberlea rhodopensis studied by means of chlorophyll fluorescence. Z Naturforsch C 61:234–240
Georgieva K, Lenk S, Buschmann C (2008) Responses of the resurrection plant Haberlea rhodopensis to high irradiance. Photosynthetica 46:208–215
Georgieva K, Doncheva S, Mihailova G, Petkova S (2012) Response of sun- and shade-adapted plants of Haberlea rhodopensis to desiccation. Plant Growth Regul 67:121–132
Ghasempour HR, Gaff DF, Williams RD, Gianello RD (1998) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul 24:185–191
Hoekstra F (2005) Differential longevities in desiccated anhydrobiotic plant systems. Integr Comp Biol 45:725–733
Illing N, Denby K, 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
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
Markovska Y, Ts T, Kimenov G, Tutekova A (1994) Physiological changes in higher poikilohydric plants—Haberlea rhodopensis Friv. and Ramonda serbica Panc. during drought and rewatering at different light regimes. J Plant Physiol 144:100–108
Morse M, Rafudeen M, Farrant JM (2011) An overview of the current understanding of desiccation tolerance in the vegetative tissues of higher plants. Adv Bot Res 57:319–347
Moyankova D, Mladenov P, Berkov S, Peshev D, Georgieva D, Djilianov D (2014) Metabolic profiling of the resurrection plant Haberlea rhodopensis during desiccation and recovery. Physiol Plant 152:675–687
Müller J, Sprenger N, Bortlik K, Boller T, Wiemken A (1997) Desiccation increases sucrose levels in Ramonda and Haberlea, two genera of resurrection plants in the Gesneriaceae. Physiol Plant 100:153–158
Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263
Oliver AE, Hincha DK, Crowe JH (2002) Looking beyond sugars: the role of amphiphilic solutes in preventing adventitious reactions in anhydrobiotes at low water contents. Comp Biochem Physiol A Mol Integr Physiol 131:515–525
Proctor MC, Tuba Z (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytol 156:327–349
Rapparini F, Neri L, Mihailova G, Petkova S, Georgieva K (2015) Growth irradiance affects the photoprotective mechanisms of the resurrection angiosperm Haberlea rhodopensis Friv. in response to desiccation and rehydration at morphological, physiological and biochemical levels. Environ Exp Bot 113:67–79
Sárvári É, Mihailova G, Solti Á, Keresztes Á, Velitchkova M, Georgieva K (2014) Comparison of thylakoid structure and organization in sun and shade Haberlea rhodopensis populations under desiccation and rehydration. J Plant Physiol 171:1591–1600
Scott P (2000) Resurrection plants and the secrets of eternal leaf. Ann Bot 85:159–166
Solti Á, Mihailova G, Sárvári É, Georgieva K (2014a) Antioxidative defence mechanisms contributes to desiccation tolerance in Haberlea rhodopensis population naturally exposed to high irradiation. Acta Biol Szeged 58:11–14
Solti Á, Lenk S, Mihailova G, Mayer P, Barócsi A, Georgieva K (2014b) Effects of habitat light conditions on the excitation quenching pathways in desiccating Haberlea rhodopensis leaves: an intelligent fluorosensor study. J Photochem Photobiol B Biol 130:217–225
Toldi O, Tuba Z, Scott P (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci 176:187–199
Van der Willigen C, Pammenter NW, Mundree SG, Farrant JM (2001) Some physiological comparisons between the resurrection grass, Eragrostis nindensis, and the related desiccation-sensitive species, Eragrostis curvula. Plant Growth Regul 35:121–129
Van der Willigen C, Pammenter NW, Mundree SC, Farrant JM (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartmentalization of subcellular components and metabolites play a role? J Exp Bot 55:651–661
Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 9:6561–6577
Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant JM (2001) Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. J Exp Bot 352:961–969
Whittaker A, Martinelli T, Bochicchio A, Vazzana C, Farrant JM (2004) Comparison of sucrose metabolism during the rehydration of desiccation-tolerant and desiccation-sensitive leaf material of Sporobolus stapfianus. Physiol Plant 122:11–20
Acknowledgments
We would like to thank to Csilla Gergely for technical assistance. This work was supported by the Bilateral Research Agreement of Bulgarian and Hungarian Academies of Sciences and the Bilateral Research Agreement of Bulgarian Academy of Sciences and National Council of Research, Italy. Á. Solti was also supported by the Bolyai János Research Scholarship of the Hungarian Academy of Sciences (BO/00207/15/4).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Néstor Carrillo
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 767 kb)
Rights and permissions
About this article
Cite this article
Georgieva, K., Rapparini, F., Bertazza, G. et al. Alterations in the sugar metabolism and in the vacuolar system of mesophyll cells contribute to the desiccation tolerance of Haberlea rhodopensis ecotypes. Protoplasma 254, 193–201 (2017). https://doi.org/10.1007/s00709-015-0932-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-015-0932-0