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A Histochemical Study of Root Nodule Development

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A Histochemical Study of Root Nodule Development A HISTOCHEMICAL STUDY OF ROOT NODULE DEVELOPMENT ONTVANGEN \ 1 JUNI 1QQ1 GêHMABiX Clemensva n deWie l CENTRALE LANDBOUW/CATALOGUS 0000 0429128 8 Promotor : Dr.A .va n Kammen,hoogleraa ri nd emoleculair e biologie Co-promotoren : Dr.A.H.J . Bisseling, universitair hoofddocent moleculaire biologie Dr.A.A.M ,va nLammeren , universitairdocen tplantencytologi e en -morfologie jUAlOpzol, WIS Clemensva n deWie l A HISTOCHEMICAL STUDY OF ROOT NODULE DEVELOPMENT Proefschrift terverkrijgin g vand egraa dva n doctori n delandbouw -e n milieuwetenschappen, op gezagva nd erecto r magnificus, dr. H.C. van der Plas, inhe topenbaa r teverdeTlige n opdinsda g 11 juni 1991 desnamiddag st evie ruu ri nd eaul a vand eLandbouwuniversitei t teWageninge n \ T'r^y- 1A( O o 5b BIBLIOTHEEK CAKDBOUWUNIVERSITJ33 KAGENINGE8 Theinvestigation s described inthi sthesi swer ecarrie dou t atth edepartmen t ofMolecula r Biology andth edepartmen t ofPlan t Cytology andMorphology , Agricultural University, Wageningen, TheNetherlands . The front cover shows adar k field micrograph of a transection through aroo t of a six- day-old pea (Pisum sativum L.) root. Expression of the PsENOD12 gene in an early stageo froo tnodul eformatio n isvisualize d byth epresenc e of white silvergrains . fJMO#E£)ft /y&s STELLINGEN 1 De integratie van moleculair-biologische en microscopische technieken leidt bij het onderzoek aan wortelknollen tot een verdieping van het inzicht in het ontwikkelingsproces. Dit proefschrift 2 Nu immunolocalisatiewaarnemingen hebben laten zien dat het voorkomen van leghemoglobine beperkt is tot de laat-symbiontische zone van de erwtewortelknol, is de waarneming van Newcomb dat de "region of thread invasion" in een "pink zone" van de wortelknol ligt, uiterst onwaarschijnlijk geworden. Newcomb(1976 )Can . J.Bot .54 : 2163. Ditproefschrif t 3 Het strijdig zijn van de immunolocalisatie van xanthinedehydrogenase (XDH) in bepaalde organellen van de ongeïnfecteerde cellen van sojawortelknollen door Nguyen et al. met observaties uit voorgaande rapporten is te verklaren door aspecifieke hechting van hun antiserum tegen XDH aan zetmeelkorrels bevattende plastiden van deongeïnfecteerd e cellen. Nguyene tal .(1986 )Plant a 167: 190. 4 Het maltraiteren van rijstwortels met celwand degraderende enzymen en poly- ethyleenglycol door Al-Mallah et al. mag dan wel leiden tot het terechtkomen van rhizobia in afgestorven cellen van een opgezwollen wortelcortex, maar heeft als zodanig weinig te maken met het aanzetten van rijst tot symbiontische wortelknolvorming. Al-Mallahe tal .(1989 )J.Exp.Bot .40 : 473. 5 Het in een onderzoek combineren van deexpertis e van tweeverschillend e vakgroepen kan vergeleken worden met het tot stand komen van een /?/jizofci«m/waardpIant- symbiose: in beide gevallen isee n uitgebalanceerde communicatiestructuur tussen de tweepartner s nodig, wil er geen voortijdige abortie plaatsvinden. Gezien de aard van de beschikbare gegevens en depraktij k van de theorievorming is het paleontologisch onderzoek naar de afstammingsgeschiedenis van de mens veel interessanter vanuit een wetenschapssociologisch dan vanuit een evolutiebiologisch oogpunt. R. Lewin (1987) Bones of contention, Simons & Schuster, Inc. D.C.Johanso n &M.A .Ede y (1981) Lucy, The beginningso f humankind,Granad aPublishing ,Ltd . De discussie overd e verwerpelijkheid van hetvogelsoortenjage n zoals gepraktizeerd door de "Dutch Birding Association" als te weinig nuttig voor natuurbescherming en/of -wetenschap getuigt van een misplaatst soort Hollands calvinisme, aangezien er uitd e aard van de bezigheid, namelijk vrije-tijdsbesteding, geen enkele aanleiding is enig nut te vooronderstellen. De discussie tussen jagers en verklaarde tegenstanders van dejach t heeft veel weg van een competentiestrijd over wie van beidepartije n de meest adequate natuurkennis ten aanzien van hetnatuurbehee r bezit. 9 In al hun diversiteit komen de plannen voor een creatief natuurbeheer, zoals het uitzetten van bevers in de Biesbosch en het plan "Ooievaar", overeen in een voorspiegeling van een terugkeer naar een soort aards paradijs, waarvan het de vraag iso f hetech t bestaan heeft en, zoja , of hetoo k ind e gewenste vorm zal terugkeren. 10 De Nederlandse Spoorwegen N.V. zouden de door hen geproclameerde aansluiting bij het huidige milieubewustzijn het beste kunnen waarmaken door de eerste- klascoupés te vervangen door ruimte voor een efficiënt en betaalbaar vervoer van fietsen ten behoeve van de verplaatsing naar en van het station. Stellingen bij het proefschrift "A histochemical study of root nodule development" door Clemens van deWiel , teverdedige n op 11 juni 1991 te Wageningen. Aan mijn ouders CONTENTS Chapter 1: Outline. 9 Chapter 2: General introduction. 13 Chapter 3: Adefenc e responseo f thehos tplan t mightinterfer e withnoduli n 35 geneexpressio n in Viciasativa roo tnodule sinduce d bya n Agrobacteriwn transconjugant. Chapter 4: Therelationshi p between nodulin geneexpressio n andth e 49 Rhizobiwn nodgene si n Viciasativa roo tnodul e development. Chapter 5: Theearl y nodulin transcriptENOD 2i slocate di nth enodul e 73 parenchyma (innercortex )o fpe aan d soybean rootnodule s Chapter 6: Nodulin geneexpressio n andENOD 2localizatio n ineffective , 91 nitrogen-fixing andineffective , bacteria-free noduleso f alfalfa (Medicagosativa) Chapter 7: TheENOD1 2gen eproduc t isinvolve d inth einfectio n process 107 during thepea-Rhizobium interaction Chapter 8: Amolecula rmarke rfo r theuninfecte d cellsi n thecentra ltissu eo f 139 pea (Piswnsativum) root nodules Chapter 9: Generaldiscussio n 155 Chapter 10: Samenvatting 177 Account 185 Nawoord 187 Curriculumvita e 189 CHAPTER 1 Outline In cooperation with soil bacteria of the genera Rhizobium, Bradyrhizobium or Azorhizobium,man y members of the legume family are ablet o form specialized organs on their roots, called root nodules. The bacteria, wrapped up inside a plant membrane, are accomodated in largeparenchymati c cells located centrally in theseroo t nodules.Fo r this,the y reward their host byconvertin g atmospheric nitrogen into afor m usable for the plant. The central infected tissue of the nodule is surrounded by a peripheral tissue provided with vascular bundles through which metabolites areexchange d with theothe r partso f theplant . Inth einteractio n with thebacteria , thehos tplan texpresse s specific genes thatar e nottranscribe d at adetectabl e leveli nothe rpart so f theplant .Th eproduct s of severalo f these genesar emad edurin g theformatio n of thenodul ean dar ename dearl ynodulins . The present study aims at elucidating the role of these early nodulins in the formation and infection of theroo t nodules.Fo r that purpose, we set out to combine the molecular approach of studying gene expression with the microscopical approach of studyingth estructura ldevelopmen to fth enodule . To provide a background to these studies, chapter II summarizes existing knowledge about nodule development from an anatomical/cytological point of view, supplemented with data on already described nodulins and with brief excursions into physiological phenomenarelevan t toth eres to f our study. In chapter III and IV, nodulin gene expression is analysed in common vetch (Vicia sativa) noduleselicite d by apane lo f bacterial strains with variousdefine d genetic changes. Such nodules were blocked atdifferen t stages in thedevelopmen t of thecentra l tissue depending on the bacterium involved; the precise stage at which the blockade occurred wasdetermine d bylight - andelectron-microscopica l observations.I ntha t way, insight could begaine d in the diverse genetic information supplied by the bacterium for nodule development to proceed through the successive developmental stages and the induction of the appropriate nodulin genes going with it. Furthermore, the start of the expression of individual nodulin genes,fo r instance theearl y nodulin Nps-40',coul d be related tocertai n stageso f central tissuedevelopment . In the caseo f the leghemoglobin genes, such acorrelatio n between nodulin gene expression and specific developmental stagescoul db econfirme d by thedirec t localization ofth eleghemoglobi n proteins inpe a (Pisum sativum) nodule sectionscomprisin g different consecutivedevelopmenta l stages, by immunolabeling. Such direct approach of studying nodulin geneexpressio n innodul e sectionswa s further pursued in the chapters V, VI, VII and VIII. In chapters V, VI and VII early nodulin gene transcripts for which sequenced cDNA clones had become available were localized by in situ hybridization: in chapter V, ENOD2 in soybean (Glycinemax) and 1 1 pea nodules, respectively; in chapter VI, ENOD2i n alfalfa (Medicago sativa) nodules; andi nchapte r VII,PsENOD1 2 inpea . Inchapte r VIII anattemp t tolocaliz e theNps-40 ' protein by immunolabeling in pea nodules is described. By these in situ localization methods,differen t temporal and spatialpattern so f geneexpressio n for eachearl y nodulin were determined. Speculations about the functions of the individual nodulins are made based upon the geneexpressio n patterns andth e amino acid sequences of thenodulin s as deduced from thenucleotid e sequenceo f thecorrespondin g cDNAclones . In addition, in chapter VI, in situ localization of MsENOD2 transcripts was performed on alfalfa nodules induced by certain engineered bacterial strainso rb y auxin transport inhibitors. Such nodules do not have bacteria in their central tissue and also differ in other structural details from effective nodules, but nevertheless
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