A Combination of Histological, Physiological, and Proteomic Approaches Shed Light on Seed Desiccation Tolerance of the Basal Angiosperm Amborella trichopoda

Villegente, Matthieu; Marmey, Philippe; Job, Claudette; Galland, Marc; Cueff, Gwendal; Godin, Benoit; Rajjou, Loïc; Zivy, Michel; Fogliani, Bruno; Sarramegna-Burtet, Valérie; Job, Dominique

doi:10.3390/proteomes5030019

Cited by 12 publications

(9 citation statements)

References 93 publications

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“…Some of the functions relating to nutrient stress responses and LD packaging are also seen even in unicellular green algae and are probably universal for CLO/PXGs [ 43 , 87 , 104 ]. However, other functions such as oxylipin-based signalling [ 105 , 106 ] are unique to multicellular organisms and probably evolved later, while other peroxygenase activities are related to the production of extracellular waxes such as cutin [ 107 – 109 ] and desiccation tolerance [ 35 , 92 , 110 ] so these functions would not have been required until plants became terrestrial. It is also becoming evident that CLO/PXGs have central roles in plant-pathogen responses, especially with fungi where the proteins may be involved in both host and pathogen crosstalk via oxylipin pathways [ 8 , 9 , 15 , 98 , 111 ].…”

Section: Resultsmentioning

confidence: 99%

Evolutionary and genomic analysis of the caleosin/peroxygenase (CLO/PXG) gene/protein families in the Viridiplantae

et al. 2018

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Bioinformatics analyses of caleosin/peroxygenases (CLO/PXG) demonstrated that these genes are present in the vast majority of Viridiplantae taxa for which sequence data are available. Functionally active CLO/PXG proteins with roles in abiotic stress tolerance and lipid droplet storage are present in some Trebouxiophycean and Chlorophycean green algae but are absent from the small number of sequenced Prasinophyceaen genomes. CLO/PXG-like genes are expressed during dehydration stress in Charophyte algae, a sister clade of the land plants (Embryophyta). CLO/PXG-like sequences are also present in all of the >300 sequenced Embryophyte genomes, where some species contain as many as 10–12 genes that have arisen via selective gene duplication. Angiosperm genomes harbour at least one copy each of two distinct CLO/PX isoforms, termed H (high) and L (low), where H-forms contain an additional C-terminal motif of about 30–50 residues that is absent from L-forms. In contrast, species in other Viridiplantae taxa, including green algae, non-vascular plants, ferns and gymnosperms, contain only one (or occasionally both) of these isoforms per genome. Transcriptome and biochemical data show that CLO/PXG-like genes have complex patterns of developmental and tissue-specific expression. CLO/PXG proteins can associate with cytosolic lipid droplets and/or bilayer membranes. Many of the analysed isoforms also have peroxygenase activity and are involved in oxylipin metabolism. The distribution of CLO/PXG-like genes is consistent with an origin >1 billion years ago in at least two of the earliest diverging groups of the Viridiplantae, namely the Chlorophyta and the Streptophyta, after the Viridiplantae had already diverged from other Archaeplastidal groups such as the Rhodophyta and Glaucophyta. While algal CLO/PXGs have roles in lipid packaging and stress responses, the Embryophyte proteins have a much wider spectrum of roles and may have been instrumental in the colonisation of terrestrial habitats and the subsequent diversification as the major land flora.

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Section: Resultsmentioning

confidence: 99%

Evolutionary and genomic analysis of the caleosin/peroxygenase (CLO/PXG) gene/protein families in the Viridiplantae

et al. 2018

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“…Another challenge facing this study is disagreement over whether seed recalcitrance or orthodoxy was the ancestral condition among angiosperm clades that first arose during the early Cretaceous (Tweddle et al, 2003;Villegente et al, 2017), because this study deals directly with fossil representatives of these groups (e.g., Wolfe and Upchurch, 1987;Upchurch, 1995). At the time that they conducted their study, seed traits of Amborellales were unknown to Wyse and Dickie (2017).…”

Section: Methodsmentioning

confidence: 99%

Seed traits linked to differential survival of plants during the Cretaceous/Paleogene impact winter

Berry¹

2020

Acta Palaeobotanica

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In past investigations the pattern of differential survival of plants across the K/Pg boundary has been viewed as incompatible with severe asteroid impact winter scenarios (i.e., an impact winter lasting more than a few months), particularly the enigmatic survival of coryphoid palms and Pandanus (screw pine). Stateof- the-art climate models based on soot, sulfate and nano-sized dust aerosols predict a global impact winter that drastically reduced precipitation and resulted in a transient period of total darkness and permafrost conditions. This suggests that the plants most likely to have been affected by the global mass-extinction event were tropical phanerophytes that produce recalcitrant seeds, which by definition are desiccation-intolerant, survive less than a year, and cannot survive freezing. However, this hypothesis has never been tested. In this study I sampled over 100 plant species from the global fossil record that have a high probability of having produced either recalcitrant seeds/disseminules (n1 = 58) or orthodox seeds (n2 = 59), based on their phylogenetic relationships with extant taxa that either are monomorphic for these traits or specifically exhibit a genetic marker for abscisic acid inhibition associated with seed dormancy and recalcitrance. A one-tailed z-test for the difference between two proportions revealed that plant taxa with a high probability of having produced recalcitrant seeds had significantly lower survivorship than plant taxa with a high probability of having produced orthodox seeds (p < 0.0001). Based on these data, it can be concluded that plants which formed a frost-tolerant seed bank during the latest Maastrichtian were significantly more likely to survive the K/Pg impact winter than plants which did not (including palms). These data clearly indicate that the K/Pg impact winter probably lasted longer than a year and that it selected for seed-based traits that effectively sorted correlated functional traits of mature plants (i.e., leaf physiognomic features). This novel hypothesis stands as an alternative to J.A. Wolfe’s classic hypothesis that a mild K/Pg impact winter selected for fast-growing angiosperms with deciduous leaves and did not affect the plant communities of the Southern Hemisphere. Potential mechanisms for the rare survival of tropical, recalcitrant-seeded plants are discussed.

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“…Key breeding objectives include improving biotic and abiotic stress resistance and enhancing yield components and seed quality, which are currently being realized through the development of genomic tools (Pandey et al, 2016;Tayeh et al, 2015;Verdier et al, 2013). In many plant species, proteomics approaches have widely been deployed to investigate the role of seed proteins in establishment of seed quality, notably concerning tolerance to desiccation and longevity (Boudet et al, 2006;Châtelain et al, 2012;Huang, Møller, & Song, 2012;Rajjou et al, 2012;Villegente et al, 2017;Wang, Liu, Song, & Møller, 2015;Wang, Møller, & Song, 2012;Yacoubi, Job, Belghazi, Chaibi, & Job, 2013); for a recent review in legumes, see Rathi, Gayen, Gayali, Chakraborty, and Chakraborty (2016). In particular, several studies highlighted the impact of protein carbonylation on seed physiological quality of a number of plant species, for example, in Arabidospsis thaliana (Job et al, 2005;Rajjou et al, 2008;Thu-Phuong, Cueff, Hegedus, Rajjou, & Bentsink, 2015), rice (Yin et al, 2017;Zhang et al, 2016;Zhang, He, Li, & Yang, 2017), wheat (Gietler, Nykiel, Orzechowski, Fettke, & Zagdańska, 2017), elm (Li, Wang, Xue, Pritchard, & Wang, 2017), sunflower (El-Maarouf-Bouteau, Meimoun, Job, Job, & Bailly, 2013;Morscher, Kranner, Arc, Bailly, & Roach, 2015;Oracz et al, 2007), apple (Debska, Krasuska, Budnicka, Bogatek, & Gniazdowska, 2013; Krasuska, Ciacka, Debska, Bogatek, & Gniazdowska, 2014), beech (Kalemba & Pukacka, 2014), upas (Bai et al, 2011), or westerner redstar (Terskikh et al, 2008).…”

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Patterns of protein carbonylation duringMedicago truncatulaseed maturation

et al. 2018

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Seeds mainly acquire their physiological quality during maturation, whereas oxidative conditions reign within cells triggering protein carbonylation. To better understand the role of this protein modification in legume seeds, we compared by proteomics patterns of carbonylated proteins in maturing seeds of Medicago truncatula naturally desiccated or prematurely dried, a treatment known to impair seed quality acquisition. In both cases, protein carbonylation increased in these seeds, accompanying water removal. We identified several proteins whose extent of carbonylation varied when comparing natural desiccation and premature drying and that could therefore be responsible for the impairment of seed quality acquisition or expression. In particular, we focused on PM34, a protein specific to seeds exhibiting a high sensitivity to carbonylation and of which function in dicotyledons was not known before. PM34 proved to have a cellulase activity presumably associated with cell elongation, a process required for germination and subsequent seedling growth. We discuss the possibility that PM34 (abundance or redox state) could be used to assess crop seed quality.

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A Combination of Histological, Physiological, and Proteomic Approaches Shed Light on Seed Desiccation Tolerance of the Basal Angiosperm Amborella trichopoda

Cited by 12 publications

References 93 publications

Evolutionary and genomic analysis of the caleosin/peroxygenase (CLO/PXG) gene/protein families in the Viridiplantae

Evolutionary and genomic analysis of the caleosin/peroxygenase (CLO/PXG) gene/protein families in the Viridiplantae

Seed traits linked to differential survival of plants during the Cretaceous/Paleogene impact winter

Patterns of protein carbonylation duringMedicago truncatulaseed maturation

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