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Balanced Xylan Acetylation Is the Key Regulator of Plant Growth and Development, and Cell Wall Structure and for Industrial Utilization

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Balanced Xylan Acetylation Is the Key Regulator of Plant Growth and Development, and Cell Wall Structure and for Industrial Utilization International Journal of Molecular Sciences Review Balanced Xylan Acetylation is the Key Regulator of Plant Growth and Development, and Cell Wall Structure and for Industrial Utilization Mirza Faisal Qaseem 1,2 and Ai-Min Wu 1,2,3,* 1 State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China; [email protected] 2 Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architectures, South China Agricultural University, Guangzhou 510642, China 3 Guangdong Laboratory of Lingnan Modern Agriculture, Guangzhou 510642, China * Correspondence: [email protected] Received: 24 September 2020; Accepted: 21 October 2020; Published: 23 October 2020 Abstract: Xylan is the most abundant hemicellulose, constitutes about 25–35% of the dry biomass of woody and lignified tissues, and occurs up to 50% in some cereal grains. The accurate degree and position of xylan acetylation is necessary for xylan function and for plant growth and development. The post synthetic acetylation of cell wall xylan, mainly regulated by Reduced Wall Acetylation (RWA), Trichome Birefringence-Like (TBL), and Altered Xyloglucan 9 (AXY9) genes, is essential for effective bonding of xylan with cellulose. Recent studies have proven that not only xylan acetylation but also its deacetylation is vital for various plant functions. Thus, the present review focuses on the latest advances in understanding xylan acetylation and deacetylation and explores their effects on plant growth and development. Baseline knowledge about precise regulation of xylan acetylation and deacetylation is pivotal to developing plant biomass better suited for second-generation liquid biofuel production. Keywords: xylan; cell wall; acetylation; deacetylation; biosynthesis; esterases 1. Introduction Xylan is the most abundant type of hemicellulose that occurs abundantly in cell walls of land plants, where it accounts for more than 30% of the dry weight, while in primary walls, it accounts for about 20% and its composition depends on the origin [1]. There is a lot of diversity in xylan structures as it depends upon the source of its origin. Generally, xylan is a heteropolymer with a backbone made of a β-(1 4)-D-xylospyranose backbone bearing 4-O-methyl-α-D-glucopyranosyl acid ! and α-L-arabinosyl and other monosaccharide side chains [2]. Depending upon the side chain on the xylan backbone, they can be divided into three major classes: glucuronoxylan, glucuronoarabinoxylan, and arabinoxylan. Glucuronoxylans are abundant in secondary walls of dicots and some non-grass monocots [2,3], glucuronoarabinoxylans are abundant in grasses and gymnosperms except members from Gnetophyta [4,5], and arabinoxylans are abundant in cereal grains [6,7]. In dicots and some non-grass monocots, glucuronoxylan made up to 25% of total weight of secondary walls. The glucuronoarabinoxylan is present in gymnosperm softwood [1] and grass species [2]. In addition, backbone may also be substituted with O-linked methyl, acetyl, and feruloyl groups which protect polysaccharides from specific glycosyl hydrolases and cross-link cell-wall constituents controlling cell extensibility [8,9]. O-Acetylation is a common and prevalent method of xylan modification and is a ubiquitous substitution within hemicellulose families [10–12]. Cell wall Int. J. Mol. Sci. 2020, 21, 7875; doi:10.3390/ijms21217875 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 7875 2 of 22 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 22 polysaccharidespolysaccharides areare eithereither mono-mono- oror di-di- acetylatedacetylated asas revealedrevealed byby aa studystudy onon tenten outout ofof fourteenfourteen cellcell wallswalls constitutingconstituting polysaccharidespolysaccharides substitutedsubstituted withwith acetylacetyl groupsgroups [[1100].]. Furthermore,Furthermore, thethe positionspositions ofof acetylationacetylation of these cell cell polysacchar polysaccharidesides also also vary, vary, for for example, example, xylose xylose in in xylan xylan is isacetylated acetylated at the at the O- O-22 and/or and/or O-3 O-3 positions, positions, galactose galactose and/or and/or mannose mannose are are acetylated acetylated at atthe the O-6 O-6 position, position, and and mannose mannose in inmannan/glucomannan mannan/glucomannan is acetylated is acetylated at the at O-2 the and/or O-2 and O-3/or positions O-3 positions [13,14]; [13 fucose,14]; fucoseat O-6 and at O-6 O-4 andand O-4galactose and galactose at the O-3 at position the O-3 in position xyloglucan in xyloglucan are also acetylated are also [15]. acetylated Acetylation [15]. of Acetylation xylan can be of of xylan four candifferent be of types, four di i.e.,fferent xylospyranose types, i.e., residues xylospyranose may be residues acetylated may at bethe acetylated 2-O position, at the and 2-O thus, position, xylan andwill thus,be called xylan 2-O-monoacetylated; will be called 2-O-monoacetylated; xylospyranose re xylospyranosesidues may be residuesacetylated may at the be acetylatedO-3 position at and the O-3thus position 3-O-monoacetylated; and thus 3-O-monoacetylated; and xylospyranose and residues xylospyranose may be acetylated residues may at both be acetylated the O-2 and at both O-3 thepositions O-2 and and O-3 thus positions regarded and as thus 2,3-di-O-acetylated. regarded as 2,3-di-O-acetylated. Finally, a xylospyranose Finally, a residue xylospyranose may contain residue an mayacetyl contain group anat the acetyl 3-O group position at theand 3-O MeGlcA position substitution and MeGlcA at position substitution O-3 is atcalled position 3-O-acetylated-2- O-3 is called 3-O-acetylated-2-MeGlcA-glycosylatedMeGlcA-glycosylated xylan. In grasses, xylan. arabinose In grasses, is attached arabinose at position is attached three atwhile position the acetyl three group while theis attached acetyl group at position is attached O-2 of at xylo positionpyronose O-2 ofresidues xylopyronose [16] (Figure residues 1). [16] (Figure1). Figure 1. Types of xylan acetylation in woody plants and grasses. Figure 1. Types of xylan acetylation in woody plants and grasses. AlthoughAlthough the the exact exact degree degree of of acetylation acetylation of cell-wall of cell-wall polymers polymers is not is yet not known, yet known, many many studies studies reveal revealthat acetylation that acetylation varies varieswith plant with planttype, type,tissue tissue type, type,developmental developmental stages, stages, and cell and wall cell wall[17–22]. [17– 22For]. Forexample, example, xylospyranose xylospyranose backbone backbone of hardwood of hardwood xylan is xylan 70% isacetylated 70% acetylated at the C-2 at and/or the C-2 C-3 and positions/or C-3 positionswhile softwood while softwoodxylospyranose xylospyranose usually lack usually acetylation lack acetylation[11]. In poplar, [11 ].as In demonstrated poplar, as demonstrated by a recent study, by a recentthe acetate study, can the reach acetate about can 6.7% reach (w/w) about of 6.7%wood (w biomass/w) of wood [23]. Similarly, biomass [different23]. Similarly, plants diorff erentplant organs plants ordiffer plant considerably organs diff iner the considerably types and content in thetypes of xylan and substitution, content of xylane.g., in substitution, the Populus trichocarpa e.g., in the stem,Populus 63% trichocarpaof the total stem,xylan 63%is acetylated, of the total of which xylan is23.6% acetylated, xylan po ofssesses which acetyl 23.6% substitution xylan possesses at the acetyl O-2 position substitution while at15.8% the O-2possesses position acetyl while substitution 15.8% possesses at the O-3 acetyl position, substitution 14.8% xylan at was the O-3substituted position, at both 14.8% the xylan O-2 and was 3 substitutedpositions, and at both9.1% thexylan O-2 has and 3Ac-2GlcA 3 positions, substitution and 9.1% [24]. xylan has 3Ac-2GlcA substitution [24]. 2.2. DiDifferencefference inin SubstitutionSubstitution PatternsPatterns ofof XylanXylan GlucuronoxylanGlucuronoxylan hashas xylospyranosexylospyranose residuesresidues inin itsits backbonebackbone connectedconnected viavia 1,4-linkages1,4-linkages andand containscontains acetyl and glucuronic glucuronic acid acid or or its its derivatives derivatives as as backbone backbone substitutions substitutions and and is iscommon common in inmany many dicots dicots [25]. [ 25In]. methylglucuronoxylan, In methylglucuronoxylan, the xylospyranose the xylospyranose backbone backbone is substituted is substituted with 4-O- withmethylgluconic 4-O-methylgluconic acid at the O-2 acid position at the O-2and has position a common and hasoccurrence a common in birch occurrence and eucalyptus in birch [19,26]. and eucalyptusThe specific [19 positions,26]. The of specific acetyl positions and methylgluconic of acetyl and acid methylgluconic on the xylan acid backbone on the xylan have backbone recently havebeen recentlydemonstrated been demonstrated in study by [27]. in study Arabinoglucuronoxylan by [27]. Arabinoglucuronoxylan and glucuronoarabinoxylan and glucuronoarabinoxylan are common are in commonthe arabinosyl in the and arabinosyl methylgluconic and methylgluconic acid groups acid at the groups O-3 atand the O-2 O-3 positions, and O-2 positions,respectively. respectively. Both are Bothdifferent are di inff erentthe content in the contentof these of two-sided these two-sided chains chainsalong with along the with acetyl the acetylcontent. content. For example,
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