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Wall Structure and Wall Loosening.

A Look Backwards and Forwards1


Daniel J. Cosgrove* Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, Pennsylvania 1 802 !"e plant #ell $all is a strong fibrillar net$ork t"at gives ea#" #ell its stable s"ape% !o enlarge, #ells se& le#tively loosen t"is net$ork, enabling it to yiel' to t"e e(pansive for#es generate' by #ell turgor pres& sure% !$enty&five years ago, #ell $all loosening $as mostly e(plore' $it"in t"e #onte(t of rapi' au(in& in'u#e' gro$t", parti#ularly in terms of t"e a#i'& gro$t" "ypot"esis )1*+ propose' in'epen'ently by ,ager in -ermany an' by .lelan' an' /ayle in t"e US0% Dis#ussion of #ell $all stru#ture #entere' on t"e influential 10lbers"eim mo'el2 first presente' by 3eegstra et al% )10+ )4ig% 10+, an' e(tension gro$t" $as $i'ely #on#eive' of as t"e result of en5ymati# "y'rolysis of matri( polysa##"ari'es )12+% !o'ay, some ne$ #"ara#ters su#" as e(pansin, (y& loglu#an en'otransgly#osylase, an' membrane& boun' en'oglu#anases "ave ma'e an entran#e into t"is s#ene, for#ing a re&evaluation of "o$ $all en& largement is #ontrolle'% !"is brief "istory summa& ri5es key #on#epts of #ell $all loosening, a topi# t"at inevitably is linke' to our vie$ of #ell $all stru#ture% EV LV!"# $ DELS F CELL WALL S%&'C%'&E Base' on sele#tive en5ymati# 'egra'ation of sy& #amore suspension #ell $alls, 3eegstra et al% )10+ propose' t"at matri( polymers, #onsisting of (ylo& glu#an, pe#ti# polysa##"ari'es, an' stru#tural pro& teins, $ere #ovalently linke' to form a giant ma#ro& mole#ular net$ork, illustrate' in 4igure 10% 6n t"is mo'el #ellulose is bon'e' to t"e matri( via ,&bon'ing to (yloglu#ans% !"is s#"eme presente' several possible sites for $all loosening% 4or instan#e, s#ission of any of t"e matri( linkages #oul' plausibly to lea' to $all e(ten& sion, sin#e t"ey are arrange' in a #"ain& link series% 3eegstra et al% also propose' t"at lo$ p, mig"t 'ire#tly $eaken t"e ,&bon'ing bet$een (yloglu#an an' #ellulose, t"ereby allo$ing mi#rofibril slippage, but subse7uent $ork from t"e same laboratory later ma'e t"is i'ea untenable% 8"en later $ork #oul' not #onfirm t"e pe#tin& (yloglu#an linkage, an alternative mo'el gaine' fa&
Copyright 2001 American Society of Plant Biologists. All rights reserved.

1 !"is $ork $as supporte' by t"e Department of 9nergy, t"e :ational S#ien#e 4oun'ation, an' t"e :ational 0eronauti#s an' Spa#e 0'ministration% ; 9&mail '#osgrove<psu%e'u= fa( 81> ? 8 @?*1A1%

vor )4ig% 1B+% 0s propose' by ,ayas"i )*+ an' 4ry ) +, #ellulose mi#rofibrils may be tet"ere' toget"er 'i& re#tly via long (yloglu#an #"ains% Pe#ti# polysa##"a& ri'es an' stru#tural proteins are imagine' as #o& e(tensive, but in'epen'ent, net$orks t"at p"ysi#ally entangle t"e #ellulose& (yloglu#an net$ork, but are not #ovalently bon'e' to it% 4ree5e&et#" repli#as of e(tra#te' $alls by M#.ann an' #olleagues )1A+ lent support to t"is mo'el% 6n a''ition, $ork by 8"itney an' #olleagues )2>+ s"o$e' t"at $"en #ellulosi# pel& li#les pro'u#e' by Acetobacter xylinum $ere gro$n in t"e presen#e of (yloglu#an or similar matri( polysa#& #"ari'es, t"e #ellulose mi#rofibrils be#ame organi5e' in a $ay t"at resemble' plant #ell $alls to a remark& able e(tent% !"ese an' ot"er results impli#ate' "emi& #elluloses as important p"ysi#al organi5ers of $all ar#"ite#ture% 0lt"oug" t"e 1tet"ere' net$ork2 mo'el of 4igure
1B is #urrently t"e most popular one )2+, ot"er vari& ations "ave been propose'% !albott an' /ay )21+ propose' a 1multi#oat2 mo'el in $"i#" ea#" mi#ro& fibril is #oate' by a series of progressively less&tig"tly boun' polysa##"ari'e layers )4ig% 1.+ an' t"e linkage

bet$een mi#rofibrils is ma'e in'ire#tly via t"e lateral )non&#ovalent+ asso#iations bet$een t"e 'istin#tive polysa##"ari'e layers% Barvis an' #olleagues )8+ #on& #eive' of a more stratifie' $all in $"i#" pe#ti# layers serve as spa#ers bet$een #ellulose&"emi#ellulose la& mellae )4ig% 1D+% !"ese pe#ti# layers ostensibly #ontrol $all t"i#kness an' allo$ for easy slippage bet$een t"e #ellulose&"emi#ellulose layers, $"i#" are t"oug"t to #ontrol $all e(tension% !"ere seems to be no 'efinitive evi'en#e at present favoring t"e tet"ere' net$ork mo'el over t"e ot"ers% /e#ent $ork "as yiel'e' ne$ evi'en#e t"at a small amount of (yloglu#an is in'ee' atta#"e' to pe#ti# polysa##"ari'es )2A+, t"us reviving t"e mo'el of 4igure 10% 8"et"er t"is pe#tin&(yloglu#an mole#u& lar fun#tions to "ol' mi#rofibrils toget"er remains to be seen% 8"at t"ese mo'els "ave in #ommon is t"e #on#ept t"at #ellulose mi#rofibrils are #oate' $it" (yloglu#an% !"e importan#e of #ellulose mi#rofibrils in $all stru#& ture $as un'ers#ore' by t"e 'is#overy of an 0rabi& 'opsis mutant $it" a 'efe#t in a gene en#o'ing a #ellulose synt"ase )1+% !"is mutant makes #ellulose,

but fails to assemble it #orre#tly into a mi#rofibril,

Plant Physiology, Banuary D2o00w1n,loCaodle% d12f@ro, mppw% w1Aw1.p? 1laAn>t,p$hy$si$ol%.polragnotpn" yes!ior"l%aorryg#D$ 220010%1 &0Pm"!erliis#haendS!oy#iwetwywo.pf lPanlat.notrgP"ysiologists

1A1

Copyright 2001 American Society of Plant Biologists. All rights reserved.

.osgrove

Figure 1. 0lternative mo'els of #ell $all stru#ture% 0, !"e mo'el of 3eegstra et al% )10+ in $"i#" t"e matri( polymers are all #ovalently linke' to one anot"er an' an#"or #ellulose by "y'rogen bon'ing to (yloglu#ans% B, !"e 1tet"ere' net$ork2 mo'el of ,ayas"i )*+ an' 4ry ) + in $"i#" single (yloglu#an #"ains span t"e gap bet$een mi#rofibrils an' tet"er t"em toget"er% !"e pe#ti# polysa##"ari'es an' stru#tural proteins are not s"o$n, but o##upy t"e spa#e bet$een (yloglu#an #"ains% ., !"e 1multi#oat2 mo'el of !albott an' /ay )21+ in $"i#" #ellulose is #oate' $it" su##essively looser layers of matri( polysa##"ari'es% D, !"e 1stratifie'2 $all mo'el of ,a et al% )8+ in $"i#" strata of pe#ti# polysa##"ari'es separate #ellulose&(yloglu#an lamellae% pm, Plasma membrane= ml, mi''le lamella% resulting in severe 'efe#ts in $all stru#ture an' or& 'ere' gro$t"% !"is 'is#overy $as also important as a #onfirmation of t"e lan'mark paper by Delmer an' #o$orkers )1E+ i'entifying t"e first #ellulose synt"ase gene in plants% 8e #an anti#ipate t"at genes en#o'& ing t"e many gly#osyl transferases re7uire' for syn& t"esis of ot"er $all polysa##"ari'es $ill be i'enti& fie'
Copyright 2001 American Society of Plant Biologists. All rights reserved.

soon )18+% $A%&!( $E%AB L!S$ A"D !%S &ELA%! " % WALL L SE"!"# !"e $all #ontains many en5ymes able to mo'ify matri( polysa##"ari'es )E+% !"ese in#lu'e various en&

'ogly#anases t"at may #leave t"e ba#kbone of an' pero(i'ases t"at may form or break p"enoli# matri( polysa##"ari'es= gly#osi'ases t"at may linkages in t"e $all% remove si'e #"ains, t"us allo$ing greater !"ese en5ymes offer many possibilities for intera#tions bet$een polysa##"ari'e ba#kbones= altering $all stru#ture, an' t"ereby mo'ulating transgly#osylases t"at may #ut polysa##"ari'es $all e(pan& sion% ,ere $e run into a subtlety of an' ligate t"em toget"er= esterases t"at #an $"at #onstitutes $all loosening% 8all "y'rolyti# remove met"yl groups from pe#& tins an' #leave en5ymes may p"ys& i#ally $eaken t"e $all, yet ester linkages bet$een polysa##"a& ri'e #"ains= not in'u#e $all e(tension Downloaded from www.plantphysiol.org on e!r"ary #$ 201% & P"!lished !y 1A www.planPt.loarngt P"ysiol% Col% 12@, 2001 2

Copyright 2001 American Society of Plant Biologists. All rights reserved.

8all Stru#ture an' 8all Loosening )A+= "en#e, t"ey 'o not #ause $all loosening by t"is 'efinition% !"e #ru#ial test is $"et"er an en5yme is #apable of in'u#ing $all e(tension% 6 "ave suggeste' t"at en5ymes $it" t"is ability be terme' primary $all loosening agents, $"ereas ot"er en5ymes t"at "ave a less 'ire#t a#tion be terme' se#on'ary $all loosening agents )i%e% t"ey mo'ify t"e $all to make it more responsive to t"e a#tion of primary $all loos& ening agents FAG+% !$enty&five years ago, au(in&in'u#e' matri( "y& 'rolysis attra#te' t"e greatest attention as a possible $all&loosening me#"anism% Matri( polysa##"ari'es e("ibit substantial "y'rolysis an' turnover in gro$& ing tissues, yet most of t"is appears to be in'epen& 'ent of e(tension gro$t"% Labavit#" an' /ay )11+ i'entifie' a (yloglu#an fra#tion $"ose turnover is spe#ifi#ally a##elerate' by au(in in 'i#ot tissues, $"ereas in grass #oleoptiles :evins an' #olleagues emp"asi5e' turnover of )1AA+,)1A>+ b&glu#an )22+% !"ese metaboli# #"anges are asso#iate' $it" in& #reases in $all plasti#ity, i%e% as measure' by stret#"& ing t"e $all in a tensile tester )12+% Moreover, $all glu#anases "ave also "ave been impli#ate' as $all& loosening agents by :evins, Masu'a, an' t"eir #ol& leagues on t"e basis of gro$t" in"ibition by antibo'& ies an' le#tins t"at interfere $it" $all "y'rolysis )22+% /e#ent $ork "as i'entifie' a novel en'o&1,A=1,>& b&glu#anase from mai5e #oleoptiles t"at is asso#iate' $it" au(in&in'u#e' matri( "y'rolysis )22+% ,o$ever, neit"er t"is nor ot"er plant en'oglu#anases "ave been s"o$n to in'u#e e(tension of $alls in vitro% Hn t"e ot"er "an', an important role for en'oglu& #anase 'uring $all assembly is in'i#ate' by an 0ra& bi'opsis mutant t"at is 'efe#tive in a gene en#o'ing a putative membrane&boun' en'oglu#anase )1@+% Be& #ause t"is en'oglu#anase is not lo#ate' in t"e $all, it probably 'oes not fun#tion as a primary $all loos& ening en5yme= rat"er, it may pro#ess $all polysa#& #"ari'es en route to $all assembly% 6n t"e past 'e#a'e (yloglu#an en'otransgly#osy& lase )I9!+ emerge' as anot"er #an'i'ate for a $all& loosening en5yme )E, 1 +% I9! is able to #ut an' ligate (yloglu#an #"ains toget"er, possibly allo$ing for a self&limiting e(tension of t"e $all% Despite t"e attra#& tiveness of t"is i'ea, I9! 'oes not in'u#e $all e(& tension in isolate' $alls )A+% I9! may fun#tion to integrate ne$ly se#rete' (yloglu#ans into t"e e(ist& ing $all net$ork )1 +% AC!D #& W%) A"D E(*A"S!"S 6n t"e 1*E0s a large bo'y of $ork establis"e' t"at plant #ells enlarge' faster $"en $all p, $as re& 'u#e' belo$ appro(imately @%@= t"is 1a#i'&
Copyright 2001 American Society of Plant Biologists. All rights reserved.

gro$t"2 be"avior $as also #"ara#teristi# of isolate' $alls an' so emerge' t"e #on#ept of a $all&loosening en5yme $it" a lo$ p, optimum% 6t $as propose' t"at t"e initial p"ase of au(in& in'u#e' gro$t" involve' a rapi' a#i'ifi#ation of t"e $all, stimulating one or

more "ypot"eti#al $all&loosening en5ymes )1*+% 6n t"e longer term au(in also stimulates $all synt"esis, in#reases $all plasti#ity, an' a#tivates genes for $all en5ymes an' ,1& 0!Pases, all of $"i#" may be im& portant fa#tors for sustaine' au(in&in'u#e' gro$t"% 0ttempts in my laboratory to i'entify $all proteins $it" t"e ability to in'u#e $all e(tension in vitro resulte' in t"e isolation of t$o a#tive proteins, later name' e(pansins )1>+% !"ese proteins me'iate t"e a#i'&in'u#e' e(tension of #u#umber "ypo#otyl $alls )A+% 8e subse7uently i'entifie' a se#on' family of e(pansins from grass pollen )@+% Members of t"is family are referre' to as b& e(pansins to 'istinguis" t"em from t"e original family of e(pansins, no$ #alle' a&e(pansins )see t"e e(pansin $eb site at $$$%bio%psu%e'uJe(pansinsJ+ % !"e t$o kin's of e(& pansins "ave similar p"ysi#al effe#ts on #ell $alls, but 'iffer in t"eir substrate preferen#es )>+% 9(pansins #"ara#teristi#ally in'u#e e(tension an' stress rela(ation of isolate' #ell $alls, but t"ey 'o not "y'roly5e t"e maKor polysa##"ari'es of t"e $all ma& tri( )1>+, nor 'o t"ey in#rease $all plasti#ity )S% Luan an' D% .osgrove, unpublis"e' 'ata+ or in#rease t"e average mobility of $all polysa##"ari'es, as mea& sure' by nu#lear magneti# resonan#e met"o's% !"us t"eir p"ysi#al effe#ts on t"e #ell $all are subtle% !"e evi'en#e for e(pansins as signifi#ant $all& loosening agents may be summari5e' as follo$s )>+M )a+ !"ey in'u#e e(tension of $alls in vitro= )b+ t"eir appli#ation to living #ells in'u#es faster

gro$t"= )#+ t"eir genes are e(presse' at t"e rig"t time an' in t"e rig"t pla#e to fun#tion in gro$t" #ontrol= an' )'+ re'u#tion of e(pansin gene e(pression by antisense met"o's results in gro$t" in"ibition% 0''itional fun#tions for e(pansin in fruit softening $ere sug& geste' by Bo#elyn /ose an' 0lan Bennett )20+ $"o foun' "ig" e(pression of an e(pansin gene 'uring t"e last stages of fruit ripening% !"e time #ourse for e(pansin a#tion is revealing, in t"at $alls begin e(ten'ing $it"in se#on's of protein a''ition, $it"out t"e lag e(pe#te' of a "y'rolyti# en5yme t"at a#ts by #"anging matri( vis#osity% 9(& pansin appears to a#t #atalyti#ally, rat"er t"an stoi& #"iometri#ally )A+% 6t #an $eaken artifi#ial #ellulosi# #omposites su#" as paper an' Acetobacter pelli#les )2@+% Hur #urrent mo'el for e(pansin a#tion proposes t"at it in'u#es slippage bet$een loa'&bearing poly& sa##"ari'es at a limite' number of sites in t"e $all )A, >+% !"is mig"t be at t"e #ellulose&(yloglu#an inter& fa#e, but t"ese interfa#es may be too abun'ant for effe#tive a#tion by e(pansin= rarer sites $it"in t"e $all seem more likely% 8"at t"ese are is still un#ertain%

A L + A)EAD 0lt"oug" $e "ave learne' mu#" in t"e past 2@ years about t"e stru#ture of t"e in'ivi'ual polymers t"at make up t"e #ell $all )2+, our i'eas of "o$ t"ey 1A Plant P"ysiol% Col% 12@, 2 0 01 D o w nloaded from www.plantphysiol.org on e!r"ary #$ A 201% & P"!lished !y www.plant.org

Copyright 2001 American Society of Plant Biologists. All rights reserved.

.osgrove form a strong yet e(tensible net$ork in t"e gro$ing $all are still base' on in'ire#t evi'en#e an' bio#"em& i#al "un#"es% More 'efinitive results in t"e future may #ome from met"o's su#" as nu#lear magneti# reso& nan#e, 4ourier transform infrare' spe#tros#opy, an' atomi# for#e mi#ros#opy, but t"e #omple(ity of t"e $all presents 'aunting #"allenges for interpreting t"e results of t"ese met"o's% 9n5ymes t"at #ut spe#ifi# sites in t"e $all )2+ offer mu#" potential for stru#tural an' me#"ani#al analyses of $all stru#ture% !"e e(& pan'ing se7uen#e 'atabases an' gro$ing resour#es for reverse geneti#s offer a''itional approa#"es for testing t"e role of spe#ifi# genes in $all stru#ture an' fun#tion% L!%E&A%'&E C!%ED 1. Arioli %, *eng L, Bet-ner AS, et al. )1**8+ S#ien#e ./01 E1E?E20
.. Car2ita "C, #i3eaut D$ )1**A+ Plant B 41 1?A0 4. Cosgrove DJ )1***+ 0nnu /ev Plant P"ysiol Plant Mol Biol 561 A*1?>1E 7. Cosgrove DJ )2000+ :ature 76/1 A21?A2 5. Cosgrove DJ, Bedinger *, Durac8ko D$ )1**E+ Pro# :atl 0#a' S#i US0 071 @@*? @ > 9. Fr: SC )1*8*+ P"ysiol Plant /51 @A2?@A /. Fr: SC )1**@+ 0nnu /ev Plant P"ysiol Plant Mol Biol 791 >*E?@20 ;. )a $A, A22erle: DC, Jarvis $C )1**E+ Plant P"ysiol

0. )a:as8i % )1*8*+ 0nnu /ev Plant P"ysiol Plant Mol Biol 761 1A*?1 8
16. +eegstra +, %al<adge +W, Bauer WD, Al3ers8ei< * )1*EA+ Plant P"ysiol 511 188?1* 11. La3avitc8 J$, &a: *$ )1*E>+ Plant P"ysiol 571 >**?@02 1.. $asuda = )1*E8+ Bot Mag !okyo 11 10A?12A 14. $cCann $C, Wells B, &o3erts + )1**2+ B Mi#ros# 1991 12A?1A 17. $c>ueen?$ason S, Durac8ko D$, Cosgrove DJ )1**2+ Plant .ell 71 1>2@?1>AA 15. "icol F, )is !, Jauneau A, Vern8ettes S, Canut ), )o@te ) )1**8+ 9MBH B 1/1 @@ A?@@E 19. "is8itani + )1**E+ 6nt /ev .ytol 1/41 1@E?20 1/. *ear J&, +awagoe =, Sc8reckengost WE, Del<er D*, Stalker D$ )1** + Pro# :atl 0#a' S#i US0 041 12 AE?12 >2 1;. *errin &$, De&oc8er AE, Bar?*eled $, Aeng W, "ora<3uena L, rellana A, &aik8el "V, +eegstra + )1***+ S#ien#e .;71 1*E ?1*E* 10. &a:le DL, Cleland &E )1**2+ Plant P"ysiol 001 12E1?12E> .6. &ose J+C, Bennett AB )1***+ !ren's Plant S#i 71 1E ?18A .1. %al3ott LD, &a: *$ )1**2+ Plant P"ysiol 0.1 A@E?A 8 ... %8o<as B&, !nou8e $, Si<<ons C&, "evins DJ )2000+ 6nt B Biol Ma#romol ./1 1>@?1>* .4. %8o<2son JE, Fr: SC )2000+ Planta .111 2E@?28 .7. W8itne: SEC, Brig8a< JE, Darke A), &eid JS#, #id? le: $J )1**@+ Plant B ;1 >*1?@0> .5. W8itne: SEC, #idle: $J, $c>ueen?$ason S )2000+

Plant B ..1 A2E?AA>

1151 @*A?@*8

Copyright 2001 American Society of Plant Biologists. All rights reserved.

Copyright 2001 American Society of Plant Biologists. All rights reserved.

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