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      Metabolic Changes on the Acquisition of Desiccation Tolerance in Seeds of the Brazilian Native Tree Erythrina speciosa

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          Abstract

          Erythrina speciosa Andrews (Fabaceae) is a native tree of Atlantic forest from Southern and Southeastern Brazil. Although this species is found in flooded areas, it produces highly desiccation tolerant seeds. Here, we investigated the physiological and metabolic events occurring during seed maturation of E. speciosa aiming to better understand of its desiccation tolerance acquisition. Seeds were separated into six stages of maturation by the pigmentation of the seed coat. Water potential (WP) and water content (WC) decreased gradually from the first stage to the last stage of maturation (VI), in which seeds reached the highest accumulation of dry mass and seed coat acquired water impermeability. At stage III (71% WC), although seeds were intolerant to desiccation, they were able to germinate (about 15%). Desiccation tolerance was first observed at stage IV (67% WC), in which 40% of seeds were tolerant. At stage V (24% WC), all seeds were tolerant to desiccation and at stage VI all seeds germinated. Increased deposition of the arabinose-containing polysaccharides, which are known as cell wall plasticizers polymers, was observed up to stage IV of seed maturation. Raffinose and stachyose gradually increased in axes and cotyledons with greater increment in the fourth stage. Metabolic profile analysis showed that levels of sugars, organic, and amino acids decrease drastically in embryonic axes, in agreement with lower respiratory rates during maturation. Moreover, a non-aqueous fractionation revealed a change on the proportions of sugar accumulation among cytosol, plastid, and vacuoles between the active metabolism (stage I) and the dormant seeds (stage VI). The results indicate that the physiological maturity of the seeds of E. speciosa is reached at stage V and that the accumulation of raffinose can be a result of the change in the use of carbon, reducing metabolic activity during maturation. This work confirms that raffinose is involved in desiccation tolerance in seeds of E. speciosa, especially considering the different subcellular compartments and suggests even that the acquisition of desiccation tolerance in this species occurs in stages prior to the major changes in WC.

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          A New Measure of Rank Correlation

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            Galactinol and raffinose constitute a novel function to protect plants from oxidative damage.

            Galactinol synthase (GolS) is a key enzyme in the synthesis of raffinose family oligosaccharides that function as osmoprotectants in plant cells. In leaves of Arabidopsis (Arabidopsis thaliana) plants overexpressing heat shock transcription factor A2 (HsfA2), the transcription of GolS1, -2, and -4 and raffinose synthase 2 (RS2) was highly induced; thus, levels of galactinol and raffinose increased compared with those in wild-type plants under control growth conditions. In leaves of the wild-type plants, treatment with 50 mum methylviologen (MV) increased the transcript levels of not only HsfA2, but also GolS1, -2, -3, -4, and -8 and RS2, -4, -5, and -6, the total activities of GolS isoenzymes, and the levels of galactinol and raffinose. GolS1- or GolS2-overexpressing Arabidopsis plants (Ox-GolS1-11, Ox-GolS2-8, and Ox-GolS2-29) had increased levels of galactinol and raffinose in the leaves compared with wild-type plants under control growth conditions. High intracellular levels of galactinol and raffinose in the transgenic plants were correlated with increased tolerance to MV treatment and salinity or chilling stress. Galactinol and raffinose effectively protected salicylate from attack by hydroxyl radicals in vitro. These findings suggest the possibility that galactinol and raffinose scavenge hydroxyl radicals as a novel function to protect plant cells from oxidative damage caused by MV treatment, salinity, or chilling.
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              The role of vitrification in anhydrobiosis.

              Numerous organisms are capable of surviving more or less complete dehydration. A common feature in their biochemistry is that they accumulate large amounts of disaccharides, the most common of which are sucrose and trehalose. Over the past 20 years, we have provided evidence that these sugars stabilize membranes and proteins in the dry state, most likely by hydrogen bonding to polar residues in the dry macromolecular assemblages. This direct interaction results in maintenance of dry proteins and membranes in a physical state similar to that seen in the presence of excess water. An alternative viewpoint has been proposed, based on the fact that both sucrose and trehalose form glasses in the dry state. It has been suggested that glass formation (vitrification) is in itself sufficient to stabilize dry biomaterials. In this review we present evidence that, although vitrification is indeed required, it is not in itself sufficient. Instead, both direct interaction and vitrification are required. Special properties have often been claimed for trehalose in this regard. In fact, trehalose has been shown by many workers to be remarkably (and sometimes uniquely) effective in stabilizing dry or frozen biomolecules, cells, and tissues. Others have not observed any such special properties. We review evidence here showing that trehalose has a remarkably high glass-transition temperature (Tg). It is not anomalous in this regard because it lies at the end of a continuum of sugars with increasing Tg. However, it is unusual in that addition of small amounts of water does not depress Tg, as in other sugars. Instead, a dihydrate crystal of trehalose forms, thereby shielding the remaining glassy trehalose from effects of the added water. Thus under less than ideal conditions such as high humidity and temperature, trehalose does indeed have special properties, which may explain the stability and longevity of anhydrobiotes that contain it. Further, it makes this sugar useful in stabilization of biomolecules of use in human welfare.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                23 October 2019
                2019
                : 10
                : 1356
                Affiliations
                [1] 1Curso de Pós-Graduação em Biodiversidade e Meio Ambiente do Instituto de Botânica de São Paulo , São Paulo, Brazil
                [2] 2Centro de Ciências Naturais e Humanas, Universidade Federal do ABC , São Bernardo do Campo, Brazil
                [3] 3Programa de Pós-Graduação em Biologia Celular e Estrutural, Universidade Estadual de Campinas (Unicamp) , Campinas, Brazil
                [4] 4BASF S.A. , Santo Antônio de Posse, Brazil
                [5] 5Department of Plant Biotechnology, Universität Stuttgart , Stuttgart, Germany
                [6] 6Núcleo de Pesquisa em Sementes, Instituto de Botânica , São Paulo, Brazil
                [7] 7Núcleo de Pesquisa em Fisiologia e Bioquímica, Instituto de Botânica , São Paulo, Brazil
                Author notes

                Edited by: Jill Margaret Farrant, University of Cape Town, South Africa

                Reviewed by: Jose Marcio Faria, Universidade Federal de Lavras, Brazil; Laura De Gara, Campus Bio-Medico University, Italy

                *Correspondence: Marcia R. Braga, bragamar@ 123456ibot.sp.gov.br ; Danilo C. Centeno, danilo.centeno@ 123456ufabc.edu.br

                This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science

                †These authors have contributed equally to this work

                Article
                10.3389/fpls.2019.01356
                6819373
                31708957
                ed34441f-47a0-4ed9-bd74-209262d98ed3
                Copyright © 2019 Hell, Kretzschmar, Simões, Heyer, Barbedo, Braga and Centeno

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 May 2019
                : 02 October 2019
                Page count
                Figures: 8, Tables: 2, Equations: 0, References: 86, Pages: 15, Words: 7411
                Funding
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo 10.13039/501100001807
                Award ID: 2005/04139-7, 2009/05369-7
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior 10.13039/501100002322
                Award ID: BEX 9389/13-0
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico 10.13039/501100003593
                Award ID: 305063/2010-3, 108991/2009-1, 478298/2011-0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                carbohydrates,cell wall,legume,metabolic profiling,non-aqueous fractionation,seed maturation

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