Gesneriads, a Source of Resurrection and Double-Tolerant Species: Proposal of New Desiccation- and Freezing-Tolerant Plants and Their Physiological Adaptations
Abstract
:Simple Summary
Abstract
1. Introduction
2. Species Identification
2.1. Phylogeny
- Sanangoideae, which did not officially become a subfamily until 2013, when it was defined as a monotypic family (Sanango racemosum) endemic to South America. It has a distinctive globose and slightly four-partite ovary with a depression in the internal structure and on top, from which the style arises surrounded by a large cupular disc [1].
- Gesnerioideae, which was initially named New World (NW) Gesneriaceae, since it was thought to contain only neotropical species. However, nowadays it also contains gesneriads from Asia and Australia, and it is considered a heterogeneous group with a well-established phylogeny [1,10]. It is generally characterized by the presence of seed endosperm, two equally sized cotyledons with limited growth, a nectary with separated glands, and an inferior ovary [11].
- Didymocarpoideae, which has been typically recognized as Old World (OW) Gesneriaceae; in this case, with the exception of Rhynchoglossum azureum, species of this subfamily are indeed found in Asia, Africa, and Europe [12,13]. The intrinsic morphological characteristics of the subfamily include the lack of endosperm, unequal cotyledon growth, ring-shaped nectary, and superior ovary [11].
2.2. Geographic Distribution and Habitat
2.2.1. Origin and Geographic Evolution of Gesneriads
2.2.2. Current Distribution and Habitat
2.3. Morphological Characterization
2.3.1. Adaptation Pressures
2.3.2. Morphological Desiccation and Freezing Tolerance Traits
2.4. Tentative Desiccation/Double-Tolerant Species
3. Physiological Adaptations for Desiccation and Freezing Tolerance
3.1. Desiccation Tolerance Strategies among Gesneriads
3.2. Avoiding Reactive Oxygen Species Formation
3.3. Avoiding Structural Damage
3.4. Cellular Protection
3.5. Freezing-Induced Desiccation
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Weber, A.; Clark, J.L.; Möller, M. A New Formal Classification of Gesneriaceae. Selbyana 2013, 31, 68–94. [Google Scholar]
- Marks, R.A.; Farrant, J.M.; Nicholas McLetchie, D.; VanBuren, R. Unexplored Dimensions of Variability in Vegetative Desiccation Tolerance. Am. J. Bot. 2021, 108, 346–358. [Google Scholar] [CrossRef] [PubMed]
- Weber, A. Gesneriaceae. In The Families and Genera of Vascular Plants; Kulbitzki, K., Ed.; Springer: Berlin, Germany, 2004; Volume 7, pp. 63–158. [Google Scholar]
- Verhoeven, A.; García-Plazaola, J.I.; Fernández-Marín, B. Shared Mechanisms of Photoprotection in Photosynthetic Organisms Tolerant to Desiccation or to Low Temperature. Environ. Exp. Bot. 2018, 154, 66–79. [Google Scholar] [CrossRef]
- Tebele, S.M.; Marks, R.A.; Farrant, J.M. Two Decades of Desiccation Biology: A Systematic Review of the Best Studied Angiosperm Resurrection Plants. Plants 2021, 10, 2784. [Google Scholar] [CrossRef]
- Clark, J.L.; Funke, M.M.; Duffy, A.M.; Smith, J.F. Phylogeny of a Neotropical Clade in the Gesneriaceae: More Tales of Convergent Evolution. Int. J. Plant Sci. 2012, 173, 894–916. [Google Scholar] [CrossRef] [Green Version]
- Serrano-Serrano, M.L.; Rolland, J.; Clark, J.L.; Salamin, N.; Perret, M. Hummingbird Pollination and the Diversification of Angiosperms: An Old and Successful Association in Gesneriaceae. Proc. R. Soc. B Biol. Sci. 2017, 284, 20162816. [Google Scholar] [CrossRef] [Green Version]
- Roalson, E.H.; Roberts, W.R. Distinct Processes Drive Diversification in Different Clades of Gesneriaceae. Syst. Biol. 2016, 65, 662–684. [Google Scholar] [CrossRef] [Green Version]
- Ogutcen, E.; Christe, C.; Nishii, K.; Salamin, N.; Möller, M.; Perret, M. Phylogenomics of Gesneriaceae Using Targeted Capture of Nuclear Genes. Mol. Phylogenet. Evol. 2021, 157, 107068. [Google Scholar] [CrossRef]
- Möller, M.; Pfosser, M.; Jang, C.G.; Mayer, V.; Clark, A.; Hollingsworth, M.L.; Barfuss, M.H.J.; Wang, Y.Z.; Kiehn, M.; Weber, A. A Preliminary Phylogeny of the “didymocarpoid Gesneriaceae” Based on Three Molecular Data Sets: Incongruence with Available Tribal Classifications. Am. J. Bot. 2009, 96, 989–1010. [Google Scholar] [CrossRef]
- Burtt, B.L.; Wiehler, H. Classification of the Family Gesneriaceae. Gesneriana 1995, 1, 1–4. [Google Scholar]
- Xu, W.; Guo, J.; Pan, B.; Zhang, Q.; Liu, Y. Diversity and Distribution of Gesneriaceae in China. Guihaia 2017, 37, 1219–1226. [Google Scholar] [CrossRef]
- Möller, M.; Wei, Y.G.; Wen, F.; Clark, J.L.; Weber, A. You Win Some You Lose Some: Updated Generic Delimitations and Classification of Gesneriaceae-Implications for the Family in China. Guihaia 2016, 35, 44–60. [Google Scholar] [CrossRef]
- Weber, A.; Middleton, D.J.; Clark, J.L.; Möller, M. Keys to the Infrafamilial Taxa and Genera of Gesneriaceae. J. Indian Assoc. Angiosperm Taxon. 2020, 30, 5–47. [Google Scholar] [CrossRef]
- Tan, K.; Lu, T.; Ren, M.X. Biogeography and Evolution of Asian Gesneriaceae Based on Updated Taxonomy. PhytoKeys 2020, 157, 26. [Google Scholar] [CrossRef] [PubMed]
- Middleton, D.J.; Atkins, H.; Truong, L.H.; Nishii, K.; Möller, M. Billolivia, a New Genus of Gesneriaceae from Vietnam with Five New Species. Phytotaxa 2014, 161, 241–269. [Google Scholar] [CrossRef]
- Wen, F.; **a, S.; Speck, T. Kinematical, Structural and Mechanical Adaptations to Desiccation in Poikilohydric Ramonda myconi (Gesneriaceae). Front. Plant Sci. 2018, 9, 1701. [Google Scholar] [CrossRef] [Green Version]
- Vieira, E.A.; Silva, K.R.; Oriani, A.; Moro, C.F.; Braga, M.R. Mechanisms of Desiccation Tolerance in the Bromeliad Pitcairnia burchellii Mez: Biochemical Adjustments and Structural Changes. Plant Physiol. Biochem. 2017, 121, 21–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heilmeier, H.; Hartung, W. Chamaegigas Intrepidus DINTER: An Aquatic Poikilohydric Angiosperm That Is Perfectly Adapted to Its Complex and Extreme Environmental Conditions. In Plant Desiccation Tolerance. Ecological Studies; Lüttge, U., Beck, E., Bartel, D., Eds.; Springer: Berlin/Heidelberg, Germany, 2011; Volume 215, pp. 233–254. [Google Scholar]
- Gaff, D.F. Desiccation Tolerant ‘Resurrection’ Grasses from Kenya and West Africa. Oecologia 1986, 70, 118–120. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Tang, M.J.; Hu, Y.L.; Lin, Z.P. Isolation and Characterization of a Dehydrin-like Gene from Drought-Tolerant Boea crassifolia. Plant Sci. 2004, 166, 1167–1175. [Google Scholar] [CrossRef]
- Fernández-Marín, B.; Nadal, M.; Gago, J.; Fernie, A.R.; López-Pozo, M.; Artetxe, U.; García-Plazaola, J.I.; Verhoeven, A. Born to Revive: Molecular and Physiological Mechanisms of Double Tolerance in a Paleotropical and Resurrection Plant. New Phytol. 2020, 226, 741–759. [Google Scholar] [CrossRef] [PubMed]
- Jovanović, Ž.; Rakić, T.; Stevanović, B.; Radović, S. Characterization of Oxidative and Antioxidative Events during Dehydration and Rehydration of Resurrection Plant Ramonda nathaliae. Plant Growth Regul. 2011, 64, 231–240. [Google Scholar] [CrossRef]
- Liu, J.; Moyankova, D.; Djilianov, D.; Deng, X. Common and Specific Mechanisms of Desiccation Tolerance in Two Gesneriaceae Resurrection Plants. Multiomics Evidences. Front. Plant Sci. 2019, 10, 1067. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drazic, G.; Mihailovic, N.; Stevanovic, B. Chlorophyll Metabolism in Leaves of Higher Poikilohydric Plants Ramonda serbica Panč, and Ramonda nathaliae Panč, et Petrov. during Dehydration and Rehydration. J. Plant Physiol. 1999, 154, 379–384. [Google Scholar] [CrossRef]
- Liu, J.; Moyankova, D.; Lin, C.T.; Mladenov, P.; Sun, R.Z.; Djilianov, D.; Deng, X. Transcriptome Reprogramming during Severe Dehydration Contributes to Physiological and Metabolic Changes in the Resurrection Plant Haberlea rhodopensis. BMC Plant Biol. 2018, 18, 351. [Google Scholar] [CrossRef]
- Georgieva, K.; Mihailova, G.; Velitchkova, M.; Popova, A. Recovery of Photosynthetic Activity of Resurrection Plant Haberlea rhodopensis from Drought-and Freezing-Induced Desiccation. Photosynthetica 2020, 58, 911–921. [Google Scholar] [CrossRef]
- Mladenov, P.; Finazzi, G.; Bligny, R.; Moyankova, D.; Zasheva, D.; Boisson, A.M.; Brugière, S.; Krasteva, V.; Alipieva, K.; Simova, S.; et al. In Vivo Spectroscopy and NMR Metabolite Fingerprinting Approaches to Connect the Dynamics of Photosynthetic and Metabolic Phenotypes in Resurrection Plant Haberlea rhodopensis during Desiccation and Recovery. Front. Plant Sci. 2015, 6, 564. [Google Scholar] [CrossRef] [Green Version]
- Asada, K. Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions. Plant Physiol. 2006, 141, 391–396. [Google Scholar] [CrossRef] [Green Version]
- Oliver, M.J.; Farrant, J.M.; Hilhorst, H.W.M.; Mundree, S.; Williams, B.; Bewley, J.D. Desiccation Tolerance: Avoiding Cellular Damage during Drying and Rehydration. Annu. Rev. Plant Biol. 2020, 71, 435–460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Georgieva, K.; Rapparini, F.; Bertazza, G.; Mihailova, G.; Sárvári, É.; Solti, Á.; Keresztes, Á. Alterations in the Sugar Metabolism and in the Vacuolar System of Mesophyll Cells Contribute to the Desiccation Tolerance of Haberlea rhodopensis Ecotypes. Protoplasma 2017, 254, 193–201. [Google Scholar] [CrossRef]
- Cañigueral, S.; Salvía, M.J.; Vila, R.; Iglesias, J.; Virgili, A.; Parella, T. New Polyphenol Glycosides from Ramonda myconi. J. Nat. Prod. 1996, 59, 419–422. [Google Scholar] [CrossRef]
- Jensen, S.R. Caffeoyl Phenylethanoid Glycosides in Sanango racemosum and in the Gesneriaceae. Phytochemistry 1996, 43, 777–783. [Google Scholar] [CrossRef]
- Feng, W.S.; Li, Y.J.; Zheng, X.K.; Wang, Y.Z.; Su, F.Y.; Pei, Y.Y. Two New C-Glycosylflavones from Boea hygrometrica. J. Asian Nat. Prod. Res. 2011, 13, 618–623. [Google Scholar] [CrossRef]
- Georgieva, K.; Dagnon, S.; Gesheva, E.; Bojilov, D.; Mihailova, G.; Doncheva, S. Antioxidant Defense during Desiccation of the Resurrection Plant Haberlea rhodopensis. Plant Physiol. Biochem. 2017, 114, 51–59. [Google Scholar] [CrossRef]
- Gechev, T.S.; Benina, M.; Obata, T.; Tohge, T.; Sujeeth, N.; Minkov, I.; Hille, J.; Temanni, M.R.; Marriott, A.S.; Bergström, E.; et al. Molecular Mechanisms of Desiccation Tolerance in the Resurrection Glacial Relic Haberlea rhodopensis. Cell. Mol. Life Sci. 2013, 70, 689–709. [Google Scholar] [CrossRef]
- Mladenov, P.V.; Zasheva, D.; Planchon, S.; Leclercq, C.; Falconet, D.; Moyet, L.; Brugière, S.; Moyankova, D.; Tchorbadjieva, M.; Ferro, M.; et al. Proteomics Evidence of a Systemic Response to Desiccation in the Resurrection Plant Haberlea rhodopensis. SSRN Electron. J. 2022, 23, 8520. [Google Scholar] [CrossRef]
- Quartacci, M.F.; Glišić, O.; Stevanović, B.; Navari-Izzo, F. Plasma Membrane Lipids in the Resurrection Plant Ramonda serbica Following Dehydration and Rehydration. J. Exp. Bot. 2002, 53, 2159–2166. [Google Scholar] [CrossRef] [Green Version]
- Moyankova, D.; Mladenov, P.; Berkov, S.; Peshev, D.; Georgieva, D.; Djilianov, D. Metabolic Profiling of the Resurrection Plant Haberlea rhodopensis during Desiccation and Recovery. Physiol. Plant 2014, 152, 675–687. [Google Scholar] [CrossRef]
- Navari-Izzo, F.; Ricci, F.; Vazzana, C.; Quartacci, M.F. Unusual Composition of Thylakoid Membranes of the Resurrection Plant Boea hygroscopica: Changes in Lipids upon Dehydration and Rehydration. Physiol. Plant 1995, 94, 135–142. [Google Scholar] [CrossRef]
- Zhu, Y.; Wang, B.; Phillips, J.; Zhang, Z.N.; Du, H.; Xu, T.; Huang, L.C.; Zhang, X.F.; Xu, G.H.; Li, W.L.; et al. Global Transcriptome Analysis Reveals Acclimation-Primed Processes Involved in the Acquisition of Desiccation Tolerance in Boea hygrometrica. Plant Cell Physiol. 2015, 56, 1429–1441. [Google Scholar] [CrossRef] [Green Version]
- Pinnola, A.; Bassi, R. Molecular Mechanisms Involved in Plant Photoprotection. Biochem. Soc. Trans. 2018, 46, 467–482. [Google Scholar] [CrossRef] [PubMed]
- Mihailova, G.; Vasileva, I.; Gigova, L.; Gesheva, E.; Simova-Stoilova, L.; Georgieva, K. Antioxidant Defense during Recovery of Resurrection Haberlea rhodopensis from Drought- and Freezing-Induced Desiccation. Plants 2022, 11, 175. [Google Scholar] [CrossRef] [PubMed]
- Mitra, J.; Xu, G.; Wang, B.; Li, M.; Deng, X. Understanding Desiccation Tolerance Using the Resurrection Plant Boea hygrometrica as a Model System. Front. Plant Sci. 2013, 4, 446. [Google Scholar] [CrossRef] [Green Version]
- Mihailova, G.; Kocheva, K.; Goltsev, V.; Kalaji, H.M.; Georgieva, K. Application of a Diffusion Model to Measure Ion Leakage of Resurrection Plant Leaves Undergoing Desiccation. Plant Physiol. Biochem. 2018, 125, 185–192. [Google Scholar] [CrossRef]
- Farrant, J.M.; Cooper, K.; Nell, H. Desiccation Tolerance. In Plant Stress Physiology; CABI: Boston, MA, USA, 2000; pp. 248–265. ISBN 9781845939953. [Google Scholar]
- Georgieva, K.; Sárvári, É.; Keresztes, Á. Protection of Thylakoids against Combined Light and Drought by a Lumenal Substance in the Resurrection Plant Haberlea rhodopensis. Ann. Bot. 2010, 105, 117–126. [Google Scholar] [CrossRef]
- Djilianov, D.; Ivanov, S.; Moyankova, D.; Miteva, L.; Kirova, E.; Alexieva, V.; Joudi, M.; Peshev, D.; van den Ende, W. Sugar Ratios, Glutathione Redox Status and Phenols in the Resurrection Species Haberlea rhodopensis and the Closely Related Non-Resurrection Species Chirita eberhardtii. Plant Biol. 2011, 13, 767–776. [Google Scholar] [CrossRef] [PubMed]
- Petrov, V.; Hille, J.; Mueller-Roeber, B.; Gechev, T.S. ROS-Mediated Abiotic Stress-Induced Programmed Cell Death in Plants. Front. Plant Sci. 2015, 6, 69. [Google Scholar] [CrossRef] [Green Version]
- Kappen, V.L. Sucht an Blättern Einiger Farne Und von Ramonda myconi. Flora 1966, 156, 427. [Google Scholar]
- Georgieva, K.; Mihailova, G.; Gigova, L.; Dagnon, S.; Simova-Stoilova, L.; Velitchkova, M. The Role of Antioxidant Defense in Freezing Tolerance of Resurrection Plant Haberlea rhodopensis. Physiol. Mol. Biol. Plants 2021, 27, 1119–1133. [Google Scholar] [CrossRef] [PubMed]
- Mihailova, G.; Solti, Á.; Sárvári, É.; Keresztes, Á.; Rapparini, F.; Velitchkova, M.; Simova-Stoilova, L.; Aleksandrov, V.; Georgieva, K. Freezing Tolerance of Photosynthetic Apparatus in the Homoiochlorophyllous Resurrection Plant Haberlea rhodopensis. Environ. Exp. Bot. 2020, 178, 104157. [Google Scholar] [CrossRef]
- Mihailova, G.; Christov, N.K.; Sárvári, É.; Solti, Á.; Hembrom, R.; Solymosi, K.; Keresztes, Á.; Velitchkova, M.; Popova, A.V.; Simova-Stoilova, L.; et al. Reactivation of the Photosynthetic Apparatus of Resurrection Plant Haberlea rhodopensis during the Early Phase of Recovery from Drought- and Freezing-Induced Desiccation. Plants 2022, 11, 2185. [Google Scholar] [CrossRef]
- Georgieva, K.; Popova, A.V.; Mihailova, G.; Ivanov, A.G.; Velitchkova, M. Limiting Steps and the Contribution of Alternative Electron Flow Pathways in the Recovery of the Photosynthetic Functions after Freezing-Induced Desiccation of Haberlea rhodopensis. Photosynthetica 2022, 60, 136–146. [Google Scholar] [CrossRef]
- Kuroki, S.; Tsenkova, R.; Moyankova, D.; Muncan, J.; Morita, H.; Atanassova, S.; Djilianov, D. Water Molecular Structure Underpins Extreme Desiccation Tolerance of the Resurrection Plant Haberlea rhodopensis. Sci. Rep. 2019, 9, 3049. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ivanova, A.; O′Leary, B.; Signorelli, S.; Falconet, D.; Moyankova, D.; Whelan, J.; Djilianov, D.; Murcha, M.W. Mitochondrial Activity and Biogenesis during Resurrection of Haberlea rhodopensis. New Phytol. 2022, 236, 943–957. [Google Scholar] [CrossRef] [PubMed]
Subtribe | Documented DT Species | Tentative Double-Tolerant/DT Species |
---|---|---|
Streptocarpinae | Streptocarpus revivescens | Streptocarpus rexii Streptocarpus meyeri Streptocarpus baudertii Streptocarpus montigena Streptocarpus rhodesianus |
Corallodiscinae | - | Corallodiscus kingianus Corallodiscus cooperi Corallodiscus bhutanicus |
Didymocarpinae | Oreocharis billburttii Oreocharis primuloides Oreocharis mileensis | Oreocharis pankaiyuae Oreocharis mairei Oreocharis ovatilobata Oreocharis flavovirens Oreocharis muscicola Oreocharis blepharophylla Oreocharis delavayi Oreocharis ninglangensis Oreocharis crispata Oreocharis magnidens Oreocharis stewardii |
Didymocarpinae | - | Henckelia incana Henckelia gambleana Henckelia fischeri Henckelia bracteata Henckelia wayanadensis Henckelia innominata |
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Legardón, A.; García-Plazaola, J.I. Gesneriads, a Source of Resurrection and Double-Tolerant Species: Proposal of New Desiccation- and Freezing-Tolerant Plants and Their Physiological Adaptations. Biology 2023, 12, 107. https://doi.org/10.3390/biology12010107
Legardón A, García-Plazaola JI. Gesneriads, a Source of Resurrection and Double-Tolerant Species: Proposal of New Desiccation- and Freezing-Tolerant Plants and Their Physiological Adaptations. Biology. 2023; 12(1):107. https://doi.org/10.3390/biology12010107
Chicago/Turabian StyleLegardón, Ane, and José Ignacio García-Plazaola. 2023. "Gesneriads, a Source of Resurrection and Double-Tolerant Species: Proposal of New Desiccation- and Freezing-Tolerant Plants and Their Physiological Adaptations" Biology 12, no. 1: 107. https://doi.org/10.3390/biology12010107