Peroxidases: evolution and expression
Associated Professor, UPS
Achraf JEMMAT (Contrat IDEX 2015-2016 => PhD student · Aix-la-Chapelle)
Sylvain Picard (M2R BioInfo 2015-2016 => CDD Hospices Civils de Lyon)
Qiang LI (doctorant chinois, financement gouvernement chinois 2010-2014). Position permanente au Citrus Research Center, Chine)
Nizar FAWAL (doctorant libanais, financement gouvernement libanais 2011-2013 => Post-doc à l’institut Pasteur, Paris)
here are two main families of peroxidases: animal peroxidases, mainly detected in animals and, by contrast, non-animal peroxidases detected in plants, fungi, bacteria and protists.
non-animal peroxidases are currently sub-divided into three classes: Class I containing the catalase-peroxidases (CP), ascorbate peroxidases (APX) and cytochrome c peroxidases (CCP); the Class II or lignin peroxidases detected only in fungi, which are able to degrade lignin; the Class III present only in plants.
The team maintains a database dedicated to peroxidases ( PeroxiBase), resulting from the manual and expert annotation of these sequences.
A noteworthy specificity of the team Evolution and Expression of peroxidase is to gather projects in bioinformatics dealing with annotation problems and evolutionary analysis of peroxidases, and projects in plant physiology , with the functional characterization of peroxidases.
- Development and update of the PeroxiBase
- Peroxidases functional analysis
- Evolutive analysis of class III peroxidases
- The ancestral peroxidase
- Cell wall plasticity
- Seed mucilage evolution
Development and update of the PeroxiBase
The initial interest to centralize sequences encoding for peroxidases from all living organisms after manual annotation and curation is still our major concern but also a guarantee of quality. However, with the increasing organisms and sequences number, the PeroxiBase needs to evolve to stay competitive and attractive.
We are aiming to develop pipelines to accelerate annotation of new peroxidases, checking and automatically correcting peroxidases annotated during the numerous genomes projects. For this, the sequences will be submitted to our family-specific profiles and also compared in terms of the exon / intron structure to the sequences present in the PeroxiBase.
In addition, it is now essential to propose specific pipeline processing sequences from NGS to make the most of this data.
Besides, new tools should be made available via the interface of the PeroxiBase to facilitate comparative analysis between organisms: mapping tools or genome browser (MapChart, GBrowse …), identification and representation of orthology or paralogy relation (SYMAP, Circos …)
Functional studies of cell wall localized CIII peroxidases during Arabidopsis thaliana development
The 73 CIII Peroxidases from Arabidopsis thaliana display specific expression profiles during development and are predicted to be targeted to the vacuole or the cell wall whether they possess or not a C-terminus vacuolar targeting sequence (Francoz et al., 2014). Recent studies indicate that the fine localization of individual peroxidases within the cell wall could provide the mean for an accurate “enzyme-substrate” meeting allowing controlled enzymatic action within cell wall micro-domains. This action can conceptually implicate either a role in cell wall loosening or in cell wall stiffening (Figure).
We are currently studying the role of CIII peroxidases – mainly cell wall localized – particularly during two developmental processes leading to the seed formation and to its germination through a transversal project involving the “Peroxidases: evolution and expression” “Cell wall proteins and Development” teams. Candidate selection is primarily based upon a pre-selection through transcriptomic data analysis followed by a second step of systematic in situ RNA hybridization. The functional study of the selected candidates displaying a specific expression profile is mainly achieved through reverse genetics with a particular interest for the ultrastructural localization of candidate proteins and for microphenotyping.
1°) Control of cell wall dynamics of seed mucilage secretory cells (MSCs) During embryogenesis, the 5 cell layers of seed coat are specialized with the outermost epidermal layer displaying a outstanding cell wall dynamism. Beside their primary cell wall, these cells develop a volcano-shaped internal secondary cell wall (the columella) and produce an abundant polysaccharidic mucilage that is compressed between the tangential primary cell wall and the columella. The role of this mucilage is only revealed during seed imbibitions several months-to-years later long after seed desiccation. Programmed localized cell wall stiffening and/or loosening events occurring during embryogenesis steps allow a polarized rupture of outer primary cell wall under the pressure of the hydrated mucilage. A mucilage pluristratified sheath decorates the seed favouring germination. We are currently studying the function, the regulation modes and the molecular targets of several CIII peroxidases during this developmental process.
2°) Control of micropylar endosperm rupture during germination The germination is controlled by external factors such as temperature, hydration and light and by hormonal equilibrium. Two major steps during germination are seed coat rupture and micropylar endosperm rupture allowing radicule protusion. Recently, the secondary messenger role of reactive oxygen species (ROS) has been demonstrated during this process (Lariguet et al., 2013). We demonstrated that ROS are produced before micropylar endosperm rupture, that ROS production is necessary for germination and that CIII peroxidases could be implicated in the spatio-temporal control of ROS production during germination. We are currently studying the function, the regulation modes and the molecular targets of several CIII peroxidases during this developmental process.
Peroxidases of class III or secreted peroxidases from plants have the characteristic of belonging to a large multigene family (73 in Arabidopsis thaliana and 138 in Oryza sativa). They are specific from plants and absent from Chlamydomonas (Chlorophyceae) and show a high rate of duplications in late divergente plants versus early divergente plants. This high rate of duplications, phylum or gender dependent, as well as gene gain and loss events, makes the evolutionary studies complex.
The comprehensive annotation of peroxidases from various plant representatives whose genomes are completely sequenced (Brachypodium, rice, Arabidopsis, sorghum, poplar …) would help to identify orthologs and events of gains and losses of genes.
Tools for sequence clustering (as orthoMCL) and reconstruction of ancestral sequences will be used to facilitate analysis.
Thus, an overall phylogenetic analysis of peroxidases in the green lineage, completed by the comparison of their gene structure and genomic organization, should allow us to understand the evolution of this complex family.
Phylogenetic tree of Class III peroxidases from Selaginella (85 seq), Arabidopsis (73 seq) and Rice (138 seq).
Looking for the ancestral peroxidase in the green lineage
Peroxidases are enzymes that catalyze reactions in which hydrogen peroxide is reduced and a variable substrate is oxidized. These proteins are present in all kingdoms and generally form gene families of varying sizes (from 2 to 138 isoforms). In plants, they have fundamental roles in various physiological processes such as detoxification of excess reactive oxygen species, defense against pathogens or the formation of cell wall (Passardi et al.; Cosio et al. 2009). Superfamily of non-animal peroxidases is widely represented in Viridiplantae. This superfamily contains three classes (classes I, II and III) with similar tertiary structures and probably shares a common ancestral sequence. Peroxidases of class I and III are found in plants. Class I peroxidases are found in all organisms containing chloroplasts, while Class III peroxidases are specific to plants and absent from Chlamydomonas. Class III as class I show a high rate of duplications in plants.
The high rate of duplication and the emergence of a particular class can be easily correlated with the emergence of terrestrial plants, with increasing oxygen level, number of pathogens and also with the structural complexity of plants. Branches such as evolutionary Charaphyceae, intermediate between Chlamydomonas and moss are interesting. Preliminary results have detected peroxidase activity of class III from Chara zeylanica. The presence of sequence (s) coding for these proteins is highly likely but unfortunately no data are available yet. The research and the specific sequencing of Class III sequence(s) of a organism from this branch industry would certainly provide answers about the evolution of non-animal peroxidases in Viridiplantae.
The project aims to (i) to choose a candidate at the base of the green strain (Charaphyceae: Nitella hyalina, Coleochaete orbicularis , Chaetospheridium globosum, Spirogyra pratensis, Penium marg, Chlorokybus atmophyticus and Klebsormidium flaccidum available from C. Delwiche’s lab web site and prepare a BAC library (screening with specific probes and sequencing of candidate) in collaboration with the CNRGV and (ii) perform a global evolutionary analysis of the non-animal peroxidases superfamily.
Cell wall plasticity in various Pyrenean altitudinal A. thaliana ecotypes
Global warming is a current concern because of its potential effects on biodiversity and the agricultural sector. A better understanding of the adaptation of plants to this recent phenomenon therefore represents a major interest for science and society. The molecular actors of the adaptation of plants to climate are little known. The walls of the plant cells represent an external barrier sensitive to environmental changes. Their structure and composition can be modified.
The objectives of this project are to evaluate Arabidopsis thaliana responses to global warming through an innovative integrative approach combining ecology, genetics, omic technologies and phenotyping data. To relate these results to a problem of global warming, these analyzes focused on natural populations coming from contrasted altitudes of the Pyrenees
An integrative approach is only possible when data as different as gene and protein expression data, weather data or phenotypic analyzes are produced. Experimental and analytical locks encountered and inherent to heterogeneous data processing have had to be removed (Hervé et al, 2016; Duruflé et al, 2017a). _Genetic and phenotypic analyzes were carried out on the new populations identified and harvested in the Pyrenees (Duruflé et al, 2017b). Moreover, the links between genetics, climatic origin and phenotypic specificity should demonstrate the distribution and natural variability of the Pyrenean populations. Two integrative studies of omic data on the theme of parietal plasticity subjected to optimal and sub-optimal temperature conditions were initiated. The first studied rosettes of two known ecotypes from contrasting growth conditions (Duruflé et al, 2017b). The second study in progress is focused on a selection of four Pyrenean populations.
By generating and combining ecological, biochemical, metabolomic and genomic data, the WallOmics project aims to understand the molecular basis of wall changes in the face of climate change by analyzing Pyrenean populations of A. thaliana from contrasted altitudes..
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Francoz E, Ranocha P, Le Ru A, Martinez Y, Fourquax I, Jauneau A, Dunand C, Burlat V, Pectin demethylesterification generates platforms that anchor peroxidases to remodel plant cell wall domains. Developmental Cell abstract
Nishiyama T et al, The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174(2):448-464 abstract
Bafoil M, Jemmat AM, Martinez Y, Merbahi N, Eichwald O, Dunand C, Yousfi M. Effects of low temperature plasmas and plasma activated waters on Arabidopsis thaliana germination and growth. PLOS One 2018 Apr 9;13(4):e0195512 abstract
Duruflé H, Hervé V, Ranocha P, Déjean S Balliau T, Zivy M, Chourré J, Burlat V, Albenne C, Jamet E, Dunand C. (2017) Cell wall adaptation of Arabidopsis, Col and Sha, to sub-optimal growth conditions : an integrative study, Plant Science 263 : 183-193 abstract
Mangano S, Denita-Juarez SP, Choi HS, Marzol E, Hwang Y, Ranocha P, Melina Velasquez S, Borassi C, Barberini ML, Aptekmann AA, Muschietti JP, Nadra AD, Dunand C, Cho HT, Estevez JM The molecular link between auxin and ROS-mediated polar growth. PNAS 114(20):5289-5294 abstract
Duruflé H, San Clemente H, Balliau T, Zivy M, Dunand C, Jamet E Cell wall proteome analysis of Arabidopsis thaliana mature stems. Proteomics 8 : abstract
Cosio C, Ranocha P, Francoz E, Burlat V, Zheng Y, Perry SE, Ripoll JJ, Yanofsky M, Dunand C (2017) The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation. New Phytol 213 : 250-263 abstract
Hervé V, Duruflé H, San Clemente H, Albenne C, Balliau T, Zivy M, Dunand C, Jamet E (2016) An enlarged cell wall proteome of Arabidopsis thaliana rosettes. Proteomics 16 : 3183-3187. abstract
Francoz E, Ranocha P, Pernot C, Le Ru A, Pacquit V, Dunand C, Burlat V. Complementarity of medium-throughput in situ RNA hybridization and tissue-specific transcriptomics : case study of Arabidopsis seed development kinetics. Scientific Reports 6:24644 abstract
Nguyen-Kim H, San Clemente H, Balliau T, Zivy M, Dunand C, Albenne C, Jamet E. Arabidopsis thaliana root cell wall proteomics : increasing the proteome coverage using a combinatorial peptide ligand library and description of unexpected Hyp in peroxidase amino acid sequences. Proteomics 16(3):491-503 abstract
Raggi S, Ferrarini A, Delledonne M, Dunand C, Ranocha P, De Lorenzo G, Cervone F, Ferrari S. The Arabidopsis Class III Peroxidase AtPRX71 Negatively Regulates Growth under Physiological Conditions and in Response to Cell Wall Damage. Plant Physiol. 2015 Dec ;169(4):2513-25. abstract
Delaux PM, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L, Rothfels CJ, Sederoff HW, Stevenson DW, Surek B, Zhang Y, Sussman MR, Dunand C, Morris RJ, Roux C, Wong GK, Oldroyd GE, Ané JM. Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci U S A. 2015 Oct 27 ;112(43):13390-5 abstract
Zhu X, Dunand C, Snedden W, Galaud JP. CaM and CMLs emergence in the green lineage. Trends Plant Sci. 2015. 20(8) 483-89 abstract
Francoz E, Ranocha P, Burlat V, Dunand C. Arabidopsis seed mucilage secretory cells : regulation and dynamics. Trends Plant Sci. 2015. 20(8) 515-24 abstract
Cao PB, Azar S, SanClemente H, Mounet F, Dunand C, Marque G, Marque C, Teulières C. Genome-wide analysis of the AP2/ERF family in Eucalyptus grandis : an intriguing over-representation of DREB1/CBF genes all stress responsive PLoS One. 2015 ;10(4):e0121041 abstract
Li Q, Yu H, Cao PB, Fawal N, Mathé C, Azar S, Cassan-Wang H, Myburg AA, Grima-Pettenati J, Marque C, Teulières C, Dunand C. Explosive tandem and segmental duplications of multigenic families in Eucalyptus grandis. Genome Biol Evol. 2015 pii : evv048 abstract
E.Francoz, P.Ranocha, H.Nguyen-Kim, E.Jamet, V.Burlat, C.Dunand. Roles of cell wall peroxidases in plant development. Phytochemistry 2015 112 : 15-21 abstract
Lauressergues D, Couzigou JM, San Clemente H, Martinez Y, Dunand, Bécard G, Combier JP. Primary transcripts of microRNAs encode regulatory peptides. Nature 2015 520(7545):90-3.abstract
Ranocha P, Francoz E, Burlat V, Dunand C. Expression of PRX36, PMEI6 and SBT1.7 is controlled by complex transcription factor regulatory networks for proper seed coat mucilage extrusion. Plant Signaling & Behavior 2014 9(11):e977734 abstract
H.Yu, M.Soler, I.Mila, H.San Clemente, C.Dunand, JAP. Paiva, AA. Myburg, M. Bouzayen, J. Grima-Pettenati and H. Cassan-Wang. Genome-wide Characterization and Expression Profiling of the AUXIN RESPONSE FACTOR (ARF) Gene Family in Eucalyptus grandis. PLoS One. 2014 9(9):e108906 abstract
Fawal N, Li Q, Mathé C, Dunand C. Automatic multigenic family annotation : risks and solutions. Trends Genet. 2014 30(8) : 323-5. abstract
Myburg AA, et al. The genome of Eucalyptus grandis. Nature. 2014 Jun 19 ;510(7505):356-62. abstract
Lariguet P, Ranocha P, De Meyer M, Barbier O, Penel C, Dunand C. Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta. 2013 238(2):381-95. abstract
Fawal N, Li Q, Savelli B, Brette M, Passaia G, Fabre M, Mathé C, Dunand C. PeroxiBase : a database for large-scale evolutionary analysis of peroxidases. Nucleic Acids Res. 2013 41(Database issue):D441-4. abstract
Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G and Séjalon-Delmas N. Origin of strigolactones in the green lineage New Phyto. 2012 195(4):857-71.abstract
Fawal, N, Savelli, B, Dunand, C, Mathé, C, GECA : a fast tool for Gene Evolution and Conservation Analysis in eukaryotic protein families. Bioinformatics. 2012 28(10):1398-9. abstract
Olson A, Aerts,A, Asiegbu F, Belbahri L, Bouzid O, Broberg A, Canbäck B, Coutinho PM, Cullen D, Dalman K, Deflorio G, van Diepen L, Dunand C, Duplessis S., Durling M., Gonthier P, Grimwood J, Gunnar Fossdal C, Hansson, D., Henrissat, B., Hietala, A., Himmelstrand, K., Hoffmeister D, Hogberg N, James T, Karlsson J, Kohler A, Kües U, Lee Y, Lin Y-C, Lind, M., Lindquist E, Lombard V, Lucas S, Lunden K, Morin E, Murat C, Park R, Raffaello T, Rouzé P, Salamov A, Schmutz J, Solheim H, Stahlberg J, Velez M, de Vries R, Wiebenga A, Woodward S, Yakovlev I, Garbelotto M, Martin F, Grigoriev I, Stenlid J Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phyto. 2012 194(4):1001-13.abstract.
Marino D, Dunand C, Puppo A and Pauly N. A burst of plant NADPH oxidases. Trends Plant Sci. 2012 17(1):9-15. abstract.
Delaux PM, Nanda AK, Mathé C, Sejalon-Delmas N, Dunand C. Molecular and biochemical aspects of plant terrestrialization. Perspective in Plant Ecology, Evolution and Systematics. 2012 14 (1), 49-59.
Dunand C, Mathé C, Lazzarotto F, Margis R, Margis-Pinheiro M. Ascorbate peroxidase-related (APx-R) is not a duplicable gene. Plant Signal Behav. 2011 6(12):1908-13. abstract.
Lazzarotto F, Teixeira FK, Barcelos Rosa S, Dunand C, Lemelle Fernandes C, de Vasconcelos Fontenele A, Silveira JAG, Verli H, Margis R, Margis-Pinheiro M. APX-R is a new heme-containing protein functionally associated to APx but evolutionarily divergent, New Phytol. 2011 191(1):234-50 abstract
Cosio C, Dunand C (2010) Transcriptome analysis of various flower and silique development stages indicates a set of class III peroxidase genes potentially involved in pod shattering in Arabidopsis thaliana. BMC Genomics 11 abstract
Mathé C, Barre A, Jourda C, Dunand C (2010) Evolution and expression of class III peroxidases. Arch Biochem Biophys 500 : 58-65 abstract
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive Oxygen Species during Plant-microorganism Early Interactions. JIPB 52 : 195-204 abstract
Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60 : 391-408 abstract
Cosio C, Vuillemin L, De Meyer M, Kevers C, Penel C, Dunand C (2009) An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta 229 : 823-836 abstract
Koua D, Cerutti L, Falquet L, Sigrist CJA, Theiler G, Hulo N, Dunand C (2009) PeroxiBase : a database with new tools for peroxidase family classification. NAR 37 : D261-D266 abstract
Oliva M, Theiler G, Zamocky M, Koua D, Margis-Pinheiro M, Passardi F, Dunand C (2009) PeroxiBase : a powerful tool to collect and analyse peroxidase sequences from Viridiplantae. J Exp Bot 60 : 453-459 abstract
Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M (2008) Glutathione peroxidase family – an evolutionary overview. FEBS J 275 : 3959-3970
Zamocky M, Jakopitsch C, Furtmuller PG, Dunand C, Obinger C (2008) The peroxidase-cyclooxygenase superfamily : reconstructed evolution of critical enzymes of the innate immune system. Proteins 72 : 589-605
Foissac S, Gouzy J, Rombauts S, Mathé C, Amselem J, Sterck L, Van de Peer Y, Rouzé P, Schiex T (2008) Genome annotation in plants and fungi : EuGene as a model platform. Current Bioinformatics 3 : 87-97
Maxime Bafoil (2018-2021). Cold Plasma and germination (co-supervisor Mohammed Yousfi, LAPLACE)
Ali Eljebbawi (2018-2021). Arabidopsis ecotypes: root phenotypes thermotolerance and salt
Sébastien Viudes (2018-2021). Brassiceae mucilage evolution (co-supervisor Vincent Burlat)
Duchesse Lacours Mbadinga Mbadinga (2017-2020). Elucidation du processus de polymérisation des monomères de cutine. Université Paul Sabatier, Toulouse III.
Harold Duruflé (2014-2017). Production et traitement de données « omics » hétérogènes en vue de l’étude de la plasticité de la paroi chez des écotypes pyrénéens de la plante modèle A. thaliana. Université Paul Sabatier, Toulouse III.
Edith Francoz (2012-2015) Rôle de la famille multigénique des peroxydases pariétales de classe III dans le développement et la dynamique des parois cellulaires végétales. Université Paul Sabatier, Toulouse III.
Qiang Li (2014) A la recherche des peroxydases ancestrales dans la lignée verte. Université Paul Sabatier, Toulouse III.
Nizar Fawal (2013) Développement d’une procédure d’annotation de familles multigéniques comme les peroxydases. Université Paul Sabatier, Toulouse III.
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