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Multiscale Investigation of Mealiness in Apple

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Multiscale Investigation of Mealiness in Apple Multiscale investigation of mealiness in apple: an atypical role for a pectin methylesterase during fruit maturation Sandrine Mikol-Segonne, Maryline Bruneau, Jean-Marc Celton, Sophie Le Gall, Mathilde Francin-Allami, Marjorie Juchaux, Francois Laurens, Mathilde Orsel Baldwin, Jean-Pierre Renou To cite this version: Sandrine Mikol-Segonne, Maryline Bruneau, Jean-Marc Celton, Sophie Le Gall, Mathilde Francin- Allami, et al.. Multiscale investigation of mealiness in apple: an atypical role for a pectin methylesterase during fruit maturation. BMC Plant Biology, BioMed Central, 2014, 14, article 375 (18 p.). 10.1186/s12870-014-0375-3. hal-01210007 HAL Id: hal-01210007 https://hal.archives-ouvertes.fr/hal-01210007 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Segonne et al. BMC Plant Biology (2014) 14:375 DOI 10.1186/s12870-014-0375-3 RESEARCH ARTICLE Open Access Multiscale investigation of mealiness in apple: an atypical role for a pectin methylesterase during fruit maturation Sandrine Mikol Segonne1, Maryline Bruneau2, Jean-Marc Celton2, Sophie Le Gall4, Mathilde Francin-Allami4, Marjorie Juchaux3, François Laurens2, Mathilde Orsel2* and Jean-Pierre Renou1,2,3* Abstract Background: Apple fruit mealiness is one of the most important textural problems that results from an undesirable ripening process during storage. This phenotype is characterized by textural deterioration described as soft, grainy and dry fruit. Despite several studies, little is known about mealiness development and the associated molecular events. In this study, we integrated phenotypic, microscopic, transcriptomic and biochemical analyses to gain insights into the molecular basis of mealiness development. Results: Instrumental texture characterization allowed the refinement of the definition of apple mealiness. In parallel, a new and simple quantitative test to assess this phenotype was developed. Six individuals with contrasting mealiness were selected among a progeny and used to perform a global transcriptome analysis during fruit development and cold storage. Potential candidate genes associated with the initiation of mealiness were identified. Amongst these, the expression profile of an early down-regulated transcript similar to an Arabidopsis thaliana pectin methylesterase gene (AtPME2) matched with mealiness development. In silico analyses of this Malus x domestica PME gene (MdPME2) confirmed its specific pattern compared with all other identified MdPME genes. Protein fusion experiments showed that MdPME2 is secreted into the apoplast in accordance with a possible activity on pectin structure. Further microscopic analysis indicated a progressive loss of cell to cell adhesion in mealy apple fruits. Biochemical analysis revealed specific modifications of pectin residues associated with mealiness, without global changes in the degree of methylesterification of pectins. Conclusions: These data support the role of PME in cell wall remodelling during apple fruit development and ripening and suggest a local action of these enzymes. Mealiness may partially result from qualitative and spatial variations of pectin microarchitecture rather than quantitative pectin differences, and these changes may occur early in fruit development. The specific MdPME2 gene highlighted in this study could be a good early marker of texture unfavourable trait in apple. Keywords: Apple, Cell wall, Malus domestica, PME, Fruit texture, Transcriptome * Correspondence: [email protected]; [email protected] 2INRA, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49071 Beaucouzé, France 1AgroCampus-Ouest, UMR 1345 Institut de Recherche en Horticulture et Semences, F-49045 Angers, France Full list of author information is available at the end of the article © 2014 Segonne et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Segonne et al. BMC Plant Biology (2014) 14:375 Page 2 of 18 Background sets in order to investigate apple fruit ripening. Most of Apple is amongst the largest consumed fruit in the world. them were based on ‘custom made’ microarrays developed During fruit maturation and ripening, apples undergo im- from EST apple databases. Lee et al. [15] used a 3,484 portant metabolic changes consisting in the conversion of cDNAs array to identify 192 cDNAs involved in the early starch to simple sugars, the reduction in organic acid con- stages of apple fruit development. Janssen et al. [16] tents, skin colour changes, production of flavoured vola- undertook a similar study on “Royal Gala” and extended tiles and flesh softening [1]. In some genotypes, mealiness to the fruit ripening stages, using a 13,000 gene apple may occur during storage. This modification in texture, oligonucleotide array. This same array was used previously often associated with excessive softening, makes apple to identify 17 putative candidate genes regulated by ethyl- fruits less attractive to consumers [2] and increases costs ene and involved in the production of aroma compounds for marketers due to a loss of quality and a higher suscep- in the fruits of transgenic lines of “Royal Gala” [17]. Costa tibility to pathogens [3,4]. et al. [18] focused on the ripening process of “Mondial Mealiness results from an undesirable ripening process Gala” using another apple EST array and heterologous and is characterized by textural deterioration, resulting hybridization using a tomato array. A high density 23 k in soft, grainy and dry fruit [5,6]. Many reports about long-oligo apple array was designed by Zhu et al. [19] to apple texture modifications during ripening have focused compare transcriptome profiles between two cultivars either on soft or mealy phenotypes. Iwanami et al. [7] with contrasted firmness and crispness phenotypes at underlined the coexistence of both phenotypes, suggesting harvest. Distinct sets of genes from various metabolic that softening studies should consider the degree of meali- pathways were classified as cultivar dependent and may ness to adequately investigate apple ripening process. contribute to the observed phenotypic variation such as Microscopic observations led to the conclusion that meali- xyloglucan endo-transglycosylase/hydrolase (XTH) genes ness is associated with the dissolution of the middle lamella involved in cell wall remodelling [10]. Other apple micro- and the disruption of the primary cell wall [5]. The authors arrays were reported on apple tree scions [20] and fruitlet suggested that these changes of the cell wall results in a abscission [21]. Until now, all published apple transcrip- loss of cell-to-cell adhesion, resulting in tissue fracture by tome studies were restricted to a subset of identified tran- cell-to-cell separation rather than by cell rupture during scripts. Due to the availability of the apple genome mastication of the fruit. Fruit cell walls are a highly com- sequence [22], the AryANE_v1 microarray representing the plex matrix composed of microfibrils of cellulose embed- fully annotated genome was recently designed [23]. ded in a network of hemicelluloses, pectins and proteins The results presented in this study constitute the first [8]. Amongst the genetically-programmed biochemical wholegenomeanalysisofappleandprovideinsightinto events which occur during fruit ripening, cell wall modifi- molecular regulatory events involved in fruit mealiness de- cations are the most described. Many enzymes are involved velopment, which is considered as the development of an in the dynamics of the cell wall during fruit development unfavourable texture trait. Up to now, the most commonly and ripening [9,10]. High α-L-arabinofuranosidase gene ex- used method to characterize mealiness was based on sen- pression and enzyme activity levels have been reported as sory analyses. As this method is rather time consuming and being related to mealiness [11]. Pectin methylesterase can be user dependent, a novel simple cell cohesion test was (PME) activity has been shown to be higher during the developed to assess mealiness. In addition, using the AryA- early stage of ripening in soft apple fruits [12]. Both en- NE_v1 microarray, six siblings from a population of hybrids zymes act on pectins (rhamnogalacturonan-I and homoga- with contrasting phenotypes for fruit mealiness were stud- lacturonan respectively) which render the cell wall matrix ied. As modifications leading to mealiness are probably initi- more accessible to other degrading enzymes such as poly- ated early in ripening, the expression profiles were studied galacturonases (PGs) [12,13]. Experiments with transgenic over the complete
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