PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification

Turbant, Amélie; Fournet, Françoise; Lequart, Michelle; Zabijak, Luciane; Pageau, Karine; Bouton, Sophie; Wuytswinkel, Olivier Van

doi:10.1093/jxb/erw025

Cited by 50 publications

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References 62 publications

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“…Pectin is synthesized in the Golgi apparatus with HGs in a fully methylesterified status (Pelloux et al, 2007; Turbant et al, 2016). The de-methylesterification by PMEs is considered to facilitate the formation of the “egg-box” structures between HG molecules and Ca 2+ , which is deemed to be associated with an increase in cell wall rigidity (Micheli, 2001; Pelloux et al, 2007; Willats et al, 2001a; Willats et al, 2001b; Wolf et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…PMEI6 , 14 , PME58 , FLY1 and SBT1.7 have been proved to be involved in HG de-methylesterification in the seed coat mucilage (Rautengarten et al, 2008; Saez-Aguayo et al, 2013; Shi et al, 2018; Turbant et al, 2016; Voiniciuc et al, 2013). In this study, we showed that PMEI13 and PMEI15 play a role in HG de-methylesterification in the seed mucilage, although PMEI15 might play only a supporting role (Supplemental Figure 9).…”

Section: Discussionmentioning

confidence: 99%

“…For example, establishing the correct degree of methylesterification (DM) is supposedly essential for mucilage extrusion and repartition upon hydration. Function defects of genes such as PMEI6 , PMEI14 , PME58 , SBT1.7 and FLY1 are assured to affect the DM, and thereby influencing mucilage structure and organization (Rautengarten et al, 2008; Saez-Aguayo et al, 2013; Turbant et al, 2016; Voiniciuc et al, 2013). In the pmei6 seeds, methylesterified HG is absent due to high PME activity, leading to mucilage release obstruction (Saez-Aguayo et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…A similar but less severe phenotype was detected for pmei14 seeds (Shi et al, 2018). On the contrary, PME58 promotes HG de-methylesterification and, in the pme58 seeds, an increase in the DM is attributed to a decrease in PME activity (Turbant et al, 2016). However, no evidence was found for interactions between PME58 and PMEI6 or PMEI14, indicating that more PMEs and PMEIs could participate in mucilage maturation, because both PME and PMEI constitute large multigene families (Turbant et al, 2016; Wang et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…On the contrary, PME58 promotes HG de-methylesterification and, in the pme58 seeds, an increase in the DM is attributed to a decrease in PME activity (Turbant et al, 2016). However, no evidence was found for interactions between PME58 and PMEI6 or PMEI14, indicating that more PMEs and PMEIs could participate in mucilage maturation, because both PME and PMEI constitute large multigene families (Turbant et al, 2016; Wang et al, 2013). The mucilage extrusion phenotype was also detected in the sbt1.7 and fly1 seeds (Rautengarten et al, 2008; Voiniciuc et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Arabidopsis ERF4 and MYB52 Transcription Factors Play Antagonistic Roles in Regulating Homogalacturonan De-methylesterification in Seed Coat Mucilage

Ding

Tang

Han

et al. 2020

Preprint

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One-sentence summary: Arabidopsis ERF4 and MYB52 transcription factors interact 18 and play antagonistic roles in regulating homogalacturonan de-methylesterification 19 related genes in the seed coat mucilage.ABSTRACT 24 The Arabidopsis (Arabidopsis thaliana) seed coat mucilage is a specialized cell wall with 25 pectin as its major component. Pectin is synthesized in the Golgi apparatus with 26 homogalacturonan fully methylesterified, but it must undergo de-methylesterification by 27 pectin methylesterase (PME) after being secreted into the cell wall. This reaction is 28 critical for pectin maturation, but the mechanisms of its transcriptional regulation remain 29 largely unknown. Here, we show that the Arabidopsis ERF4 transcription factor 30 positively regulates pectin de-methylesterification during seed development and directly 31 suppresses the expression of PME INHIBITOR13 (PMEI13), 14, 15 and 32 SUBTILISIN-LIKE SERINE PROTEASE 1.7 (SBT1.7). The erf4 mutant seeds showed 33 repartitioning of mucilage between soluble and adherent layers as a result of decreased 34 PME activity and increased degree of pectin methylesterification. ERF4 physically 35 associates with and antagonizes MYB52 in activating PMEI6, 14 and SBT1.7 and 36 MYB52 also antagonizes ERF4 activity in the regulation of downstream targets. Gene 37 expression studies revealed that ERF4 and MYB52 have opposite effects on pectin 38 de-methylesterification. Genetic analysis indicated that the erf4-2 myb52 double mutant 39 seeds show mucilage phenotype similar to wild-type. Taken together, this study 40 demonstrates that ERF4 and MYB52 antagonize each other's activity to maintain the 41 appropriate degree of pectin methylesterification, expanding our understanding of how 42 pectin de-methylesterification is fine-tuned by the ERF4-MYB52 transcriptional complex 43 in the seed mucilage. 44 130 6 stress (Liu et al., 2017). ERF4 is expressed ubiquitously in Arabidopsis (Winter et al., 131 2007), suggesting that it has other functions in addition to those mentioned above. For 132 example, its regulatory role in cell wall biology has not been reported yet. 133Here, we provide evidence that ERF4 positively regulates pectin de-methylesterification 134 in the seed mucilage. We find a repartitioning of seed mucilage polysaccharides in the 135 erf4 seeds under vigorous shaking conditions which can be attributed to an increase in 136 DM. ERF4 binds to the cis-regulatory elements and directly suppresses the expression of 137 PMEI13, 14, 15 and SBT1.7. Moreover, ERF4 and MYB52 were found to interact, and 138 play completely opposite roles in pectin de-methylesterification by antagonizing each 139 other's transcriptional activity, which is confirmed by gene expression and genetic 140 evidence. Overall, these findings provide a fine-tuned mechanism where ERF4 and 141 MYB52 antagonistically control mucilage modification related genes. 142 RESULTS 143Expression pattern of ERF4 is correlated with seed mucilage deposition 144 Previous studies revea...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Arabidopsis ERF4 and MYB52 Transcription Factors Play Antagonistic Roles in Regulating Homogalacturonan De-methylesterification in Seed Coat Mucilage

Ding

Tang

Han

et al. 2020

Preprint

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New Insights into the Composition and Structure of Seed Mucilage

Phan

Burton

2018

Annual Plant Reviews Online

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Upon exposure to aqueous environments, polysaccharides present in the seed coats of myxospermous species swell and extrude forming a halo of mucilage that completely envelops the seed. The extruded mucilage is usually a composite of pectic, non‐cellulosic, and cellulosic polysaccharides, and because of its accessibility the seed mucilage system has been used extensively in the laboratory to uncover molecular mechanisms associated with plant cell wall (PCW) polysaccharide biosynthesis. The mucilage of Arabidopsis , which is predominantly composed of pectic polysaccharides, is the most extensively characterised. Interrogation of this system has revealed intricate molecular and chemical details about polysaccharide biosynthesis and seed coat development, clearly demonstrating the effectiveness of using seed mucilage systems as a proxy to study PCW polysaccharide biosynthesis. Significant advances have been made in our understanding and identification of the genes and enzymes involved in pectin, cellulose, and xylan biosynthesis. Recent results regarding the composition, combined with the definition of the architectural properties, of extruded seed mucilage are synergistic with our current models of how polysaccharides interact in the PCW. In addition to the desirable characteristics of myxospermy for the study of PCW polysaccharide biosynthesis, industrial applications of seed mucilages are extensive. Strong interest from the food manufacturing and processing, pharmaceutical, cosmetic, and waste management industries has also encouraged researchers to investigate the physiochemical properties of seed mucilages and their possible applications. This article highlights the recent advances made in our understanding of the molecular mechanisms and the architectural properties of mucilage biosynthesis across diverse species.

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Arabidopsis Seed Mucilage: A Specialised Extracellular Matrix that Demonstrates the Structure–Function Versatility of Cell Wall Polysaccharides

Šola

Dean

Haughn

2019

Annual Plant Reviews Online

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Arabidopsis seed coat mucilage is a specialised extracellular matrix composed of the same broad classes of polysaccharides found in a primary cell wall (cellulose, pectin, and hemicellulose), arranged in a distinct structure with special properties. It is deposited by the seed coat epidermal cells in the apoplast in a polar manner to produce a doughnut‐shaped mucilage pocket on the outside of the cell. Following exposure to water the mucilage extrudes from the outer surface of the cell. A portion of this mucilage remains strongly adherent to the seed. The unique features of mucilage make it amenable to study, and genetic, cytological, and biochemical analyses have been used to determine its composition, synthesis, and structure, and establish how these combine to determine its properties. Lessons learned from these studies strengthen and extend our understanding of plant extracellular matrices, especially the cell wall. In this article, we summarise and contextualise what is currently known about mucilage by focusing on its main features – extrusion and adherence.

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PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification

Abstract: Highlight PME58 is the first pectin methylesterase gene identified to play a direct role in seed coat mucilage structure. Its activity influences pectin distribution upon mucilage extrusion.

Cited by 50 publications

References 62 publications

Arabidopsis ERF4 and MYB52 Transcription Factors Play Antagonistic Roles in Regulating Homogalacturonan De-methylesterification in Seed Coat Mucilage

Arabidopsis ERF4 and MYB52 Transcription Factors Play Antagonistic Roles in Regulating Homogalacturonan De-methylesterification in Seed Coat Mucilage

New Insights into the Composition and Structure of Seed Mucilage

Arabidopsis Seed Mucilage: A Specialised Extracellular Matrix that Demonstrates the Structure–Function Versatility of Cell Wall Polysaccharides

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