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      Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness

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          Abstract

          Somatic embryogenesis (SE) is the most striking and prominent example of plant plasticity upon severe stress. Inducing immature carrot seeds perform SE as substitute to germination by auxin treatment can be seen as switch between stress levels associated to morphophysiological plasticity. This experimental system is highly powerful to explore stress response factors that mediate the metabolic switch between cell and tissue identities. Developmental plasticity per se is an emerging trait for in vitro systems and crop improvement. It is supposed to underlie multi-stress tolerance. High plasticity can protect plants throughout life cycles against variable abiotic and biotic conditions. We provide proof of concepts for the existing hypothesis that alternative oxidase (AOX) can be relevant for developmental plasticity and be associated to yield stability. Our perspective on AOX as relevant coordinator of cell reprogramming is supported by real-time polymerase chain reaction (PCR) analyses and gross metabolism data from calorespirometry complemented by SHAM-inhibitor studies on primed, elevated partial pressure of oxygen (EPPO)–stressed, and endophyte-treated seeds. In silico studies on public experimental data from diverse species strengthen generality of our insights. Finally, we highlight ready-to-use concepts for plant selection and optimizing in vivo and in vitro propagation that do not require further details on molecular physiology and metabolism. This is demonstrated by applying our research & technology concepts to pea genotypes with differential yield performance in multilocation fields and chickpea types known for differential robustness in the field. By using these concepts and tools appropriately, also other marker candidates than AOX and complex genomics data can be efficiently validated for prebreeding and seed vigor prediction.

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          Two Faces of One Seed: Hormonal Regulation of Dormancy and Germination.

          Seed plants have evolved to maintain the dormancy of freshly matured seeds until the appropriate time for germination. Seed dormancy and germination are distinct physiological processes, and the transition from dormancy to germination is not only a critical developmental step in the life cycle of plants but is also important for agricultural production. These processes are precisely regulated by diverse endogenous hormones and environmental cues. Although ABA (abscisic acid) and GAs (gibberellins) are known to be the primary phytohormones that antagonistically regulate seed dormancy, recent findings demonstrate that another phytohormone, auxin, is also critical for inducing and maintaining seed dormancy, and therefore might act as a key protector of seed dormancy. In this review, we summarize our current understanding of the sophisticated molecular networks involving the critical roles of phytohormones in regulating seed dormancy and germination, in which AP2-domain-containing transcription factors play key roles. We also discuss the interactions (crosstalk) of diverse hormonal signals in seed dormancy and germination, focusing on the ABA/GA balance that constitutes the central node.
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            Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis.

            The transition from dormancy to germination in seeds is a key physiological process during the lifecycle of plants. Abscisic acid (ABA) is the sole plant hormone known to maintain seed dormancy; it acts through a gene expression network involving the transcription factor ABSCISIC ACID INSENSITIVE 3 (ABI3). However, whether other phytohormone pathways function in the maintenance of seed dormancy in response to environmental and internal signals remains an important question. Here, we show that the plant growth hormone auxin, which acts as a versatile trigger in many developmental processes, also plays a critical role in seed dormancy in Arabidopsis. We show that disruptions in auxin signaling in MIR160-overexpressing plants, auxin receptor mutants, or auxin biosynthesis mutants dramatically release seed dormancy, whereas increases in auxin signaling or biosynthesis greatly enhance seed dormancy. Auxin action in seed dormancy requires the ABA signaling pathway (and vice versa), indicating that the roles of auxin and ABA in seed dormancy are interdependent. Furthermore, we show that auxin acts upstream of the major regulator of seed dormancy, ABI3, by recruiting the auxin response factors AUXIN RESPONSE FACTOR 10 and AUXIN RESPONSE FACTOR 16 to control the expression of ABI3 during seed germination. Our study, thus, uncovers a previously unrecognized regulatory factor of seed dormancy and a coordinating network of auxin and ABA signaling in this important process.
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              Mitochondrial control of cellular life, stress, and death.

              Since the discovery that mitochondrial membrane permeabilization represents a critical step in the regulation of intrinsic apoptosis, mitochondria have been viewed as pluripotent organelles, controlling cell death as well as several aspects of cell survival. Mitochondria constitute the most prominent source of ATP and are implicated in multiple anabolic and catabolic circuitries. In addition, mitochondria coordinate cell-wide stress responses, such as autophagy, and control nonapoptotic cell death routines, such as regulated necrosis. Thus, mitochondria seem to regulate a continuum of cellular functions, spanning from physiological metabolism to stress responses and death. The involvement of mitochondria in both vital and lethal processes is crucial for both embryonic and postembryonic development, as well as for the maintenance of adult tissue homeostasis. In line with this notion, primary mitochondrial defects or alterations in the signaling pathways that converge on or emanate from mitochondria underpin a large number of human diseases, including premature aging, neurodegenerative disorders, cardiovascular disorders, and cancer. Here, we provide an overview of the molecular mechanisms that enable mitochondria to sustain cell survival, coordinate stress responses, and mediate cell death, linking these pathways--whenever relevant--to cardiovascular health and disease.
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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
                20 September 2019
                2019
                : 10
                : 1134
                Affiliations
                [1] 1Plant Genetic Engineering Laboratory, Department of Biotechnology, Bharathiar University , Coimbatore, India
                [2] 2Functional Cell Reprogramming and Organism Plasticity (FunCROP), University of Évora , Évora, Portugal
                [3] 3Cell and Molecular Biology of Plants (BPOCEMP)/Industrial Biotechnology and Bioproducts, Department of Sciences of the Vidaydela Agriculture, University of the Armed Forces-ESPE , Milagro, Ecuador
                [4] 4Faculty of Engineering, State University of Milagro (UNEMI) , Milagro, Ecuador
                [5] 5Functional Genomics and Bioinformatics Group, Department of Biochemistry and Molecular Biology, Federal University of Ceará , Fortaleza, Brazil
                [6] 6Council for Agricultural Research and Economics (CREA), Research Centre for Animal Production and Aquaculture , Lodi, Italy
                [7] 7Wageningen Plant Research, Wageningen University & Research , Wageningen, Netherlands
                [8] 8National Institute of Plant Genome Research , New Delhi, India
                [9] 9CERNAS-Research Center for Natural Resources, Environment and Society, Department of Environment, Escola Superior Agrária de Coimbra , Coimbra, Portugal
                Author notes

                Edited by: Sandra Isabel Correia, University of Coimbra, Portugal

                Reviewed by: Elena Corredoira, Instituto de Investigaciones Agrobiológicas de Galicia (IIAG), Spain; Taras P. Pasternak, University of Freiburg, Germany

                *Correspondence: Birgit Arnholdt-Schmitt, eu_chair@ 123456uevora.pt ; Ramalingam Sathishkumar, rsathish@ 123456buc.edu.in

                This article was submitted to Plant Development and EvoDevo, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.01134
                6776121
                e3eb2342-8532-4b1c-94ab-76ca79ce4f63
                Copyright © 2019 Mohanapriya, Bharadwaj, Noceda, Costa, Kumar, Sathishkumar, Thiers, Santos Macedo, Silva, Annicchiarico, Groot, Kodde, Kumari, Gupta and Arnholdt-Schmitt

                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
                : 06 April 2019
                : 16 August 2019
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 99, Pages: 11, Words: 5131
                Categories
                Plant Science
                Perspective

                Plant science & Botany
                environmental stress,developmental plasticity,metabolic biomarker,endophytes,seed technology,plant performance prediction

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