TO produce organs predictably, meristems tightly
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1 Copyright Ó 2009 by the Genetics Society of Americ DOI: /genetics Note The Interction of knotted1 nd thick tssel dwrf1 in Vegettive nd Reproductive Meristems of Mize Chin Lunde nd Srh Hke 1 Plnt Gene Expression Center, University of Cliforni, Berkeley, Cliforni nd United Sttes Deprtment of Agriculture Agriculturl Reserch Service, Albny, Cliforni Mnuscript received November 5, 2008 Accepted for publiction Jnury 8, 2009 ABSTRACT In Arbidopsis, SHOOT MERISTEMLESS (STM) nd CLAVATA1 (CLV1) competitively regulte meristem homeostsis. Here, we explore the interction of their mize homologs knotted1 (kn1) nd thick tssel dwrf1 (td1). kn1 mutnts form fewer lterl orgns nd td1 inflorescences re fscited with dditionl florl orgns. Double mutnts show kn1 episttic to td1 in seedling nd er development but dosesensitivity exists lter to promote lef initition. Thus kn1 nd td1 function in pthwy to mintin meristem homeostsis but their products my interct with different prtners during development. TO produce orgns predictbly, meristems tightly control the opposing processes of meristem mintennce nd lterl orgn initition. In Arbidopsis, the CLAVATA (CLV) genes control blnce between these processes. Loss-of-function/hypomorphic clv mutnts hve enlrged shoot nd florl meristems, producing more florl orgns (Leyser nd Furner 1992; Clrk et l. 1993, 1995; Kyes nd Clrk 1998). CLV1 nd CLV2 encode leucine-rich repet (LRR) receptor-like kinse protein nd n LRR protein lcking kinse domin, respectively (Clrk et l. 1997; Jeong et l. 1999). CLV3 encodes smll peptide (Fletcher et l. 1999) tht physiclly intercts with CLV1 (Ogw et l. 2008). BAM1, BAM2, nd BAM3 encode CLV1-relted receptor kinses. Opposite of clv mutnts, the double or triple bm mutnts hve smller meristems (DeYoung et l. 2006). Genetic evidence, however, points to significnt role for the BAM loci in the CLV pthwy, s the bm mutnts meliorte the clv3 phenotype but enhnce null lleles of clv1 (DeYoung nd Clrk 2008). The homeobox gene SHOOT MERISTEMLESS (STM), centrl to meristem mintennce nd determincy (Long et l. 1996), functions in seprte pthwy (Brnd et l. 2002; Lenhrd et l. 2002). Strong stm mutnts lck vegettive development nd produce only cotyledons (Brton nd Poethig 1993). Wek stm mutnts my progress to flowering nd demonstrte 1 Corresponding uthor: U.S. Deprtment of Agriculture ARS, 800 Buchnn St., Albny, CA E-mil: mizesh@nture.berkeley.edu function for STM in inflorescences (Endrizzi et l. 1996; Brnd et l. 2002; Bhtt et l. 2004; Knrr et l. 2006). clv1 lleles suppress the stm phenotype nd stm lleles suppress the clv1 phenotype, indicting tht these genes ply ntgonistic roles. This genetic interction is dose dependent: CLV1 nd STM proteins re sensitive to ech other, suggesting tht their blnce is necessry to mintin proper meristem size nd shpe (Clrk et l. 1996). Knotted1 (kn1) is mize homolog of STM with similr expression pttern nd function (Smith et l. 1992; Vollbrecht et l. 2000). Expressivity of recessive kn1 muttions depends upon genetic bckground nd meristem size. In inbred lines with lrger meristems, defects re most pronounced during the dult phse: tssels re less brnched, ers often bsent or with reduced seed set. Ectopic leves my form bove the er node (Kerstetter et l. 1997). In restrictive bckgrounds with smller meristems, limited shoot phenotype is seen in which zero to two leves form (Vollbrecht et l. 2000). clv-like muttions ffect distinct meristems in the grsses, unlike Arbidopsis, in which ll shoot meristems re lrger. Muttions in the CLV3 rice homolog, FON2, ffect only florl meristems (Suzki et l. 2006), while muttions in nother CLV3 homolog, FCP1, ffect only vegettive meristems (Suzki et l. 2008). Muttions in the rice CLV1 homolog, FON1, ffect only florl meristems (Suzki et l. 2004), suggesting nother CLV1 homolog functions in inflorescence nd vegettive meristems. thick tssel dwrf (td1) encodesthemost similr mize CLV1 homolog with 58% mino cid Genetics 181: (April 2009)
2 1694 C. Lunde nd S. Hke TABLE 1 Penetrnce of limited shoot phenotype in the B73:Mo17 genetic bckground Genotype N LS b (n) kn1/kn1; td1/td c kn1/kn1; td1/ kn1/kn1; 1/1 7 1 c kn1/1; td1/td kn1/1; td1/ kn1/1; 1/1 5 0 Totl 68 8 To crete fmily segregting double mutnts in the B73:Mo17 bckground, kn1-e1 ws bckcrossed to Mo17 four times nd td1-glf ws bckcrossed to B73 nine times. An F 1 plnt with these two prents ws self-pollinted to mke n F 2 fmily nd ssyed by PCR for ll possible llelic combintions. Only kn1-e1 plnts showed the limited shoot phenotype. An F 2 individul with the genotype kn1-e1/1 td1-glf/1 ws crossed to sibling with the genotype kn1-e1/kn1-e1 td1-glf/1 to enrich for double mutnts. Plnts were grown under greenhouse conditions. Not significntly different from expected rtio (X 2, P. 0.01). b Limited shoot phenotype. c One plnt in ech of these clsses recovered nd grew normlly. identity to CLV1 nd 51% identity to BAM1 nd BAM2. td1 mutnts hve enlrged inflorescence meristems, incresed spikelet density nd supernumerry florl orgns but, in contrst, reduced vegettive growth. Plnts re shorter with fewer leves (Bommert et l. 2005). Thus TD1 my promote vegettive meristem growth nd restrict inflorescence nd florl meristem growth. To investigte the role of STM- nd CLV1-homologous pthwys in the grsses, we hve utilized muttions in kn1 nd td1 to observe double-mutnt phenotypes. td1-glf fils to suppress the limited shoot phenotype of kn1-e1: We combined the null kn1-e1 llele (Vollbrecht et l. 2000) with the null td1-glf llele (Bommert et l. 2005) to determine if td1-glf cn suppress the limited shoot phenotype cused by kn1-e1. The limited shoot phenotype ws more penetrnt in mixed B73:Mo17 bckground thn in B73 lone, llowing us to study more individuls. Of 39 kn1-e1 homozygous plnts, 8 (20.5%) exhibited limited shoots (Tble 1; Figure 1A). The genotype t the td1 locus did not ffect this phenotype, indicting tht td1-glf cnnot suppress the effects of kn1-e1 during erly vegettive growth nd tht kn1-e1 is episttic to td1-glf. td1-glf vegettive meristems re smller: In Arbidopsis, clv1 meristems re lrger thn wild type during vegettive growth (Clrk et l. 1993). In contrst, we found tht vegettive meristems of td1-glf mutnts re smller thn those of wild-type siblings (Figure 2). This finding my explin why td1-glf does not suppress kn1-e1. td1-glf increses the penetrnce of the kn1-e1 ectopic vegettive lef phenotype: In permissive bckgrounds, plnts homozygous for kn1 loss-of-function lleles develop ectopic leves in the xils of leves t low penetrnce (12%) (Kerstetter et l. 1997). td1-glf enhnced this phenotype dose dependently (Tble 2) (Figure 1, B E). The ectopic leves re reversed in polrity with their dxil surfce (Figure 1D) fcing the dxil surfce of the true lef. In n F 2 fmily segregting td1-glf nd kn1-e1, ll double mutnts hd t lest one ectopic lef, while kn1-e1 homozygotes with one or no copies of td1-glf hd 40% nd 20%, respectively. In fmily segregting 50% kn1-e1 nd 50% kn1-e1/1 in the td1- glf mutnt bckground, 90% of double mutnts nd 40% of kn1-e1 heterozygotes hd ectopic leves. No kn1- E1/1 td1-glf/td1-glf plnts hd ectopic leves in the F 2 fmily, indicting possible epigenetic nd/or environmentl influence on the phenotype. We lso observed fusion of most ectopic leves of double mutnts to the djcent lef (Figure 1E) wheres fusion only occurred in qurter of ectopic leves of kn1-e1/1 td1-glf/td1-glf plnts. Thus, we detected synergistic increse in penetrnce of ectopic leves nd n unexpected involvement of td1 in the regultion of lef initition. kn1-e1 is episttic to td1-glf in er development: kn1 nd td1 re ntgonistic in er development. In permissive bckgrounds, ers of kn1 mutnts re smll with reduced spikelet density (Kerstetter et l. 1997). Ers of td1 mutnts re fscited with incresed spikelet Figure 1. Vegettive phenotypes of double mutnts. (A) A kn1-e1; td1-glf seedling showing the limited shoot phenotype of single lef. Norml siblings re in the bckground. Their first lef hs senesced. (B) An ectopic lef in the xil of norml lef. The ligule (rrow) is fcing the ligule of the norml lef (not seen). The ectopic lef is ttched t the meristem. (C D) Ech surfce of ectopic lef from B. (E) A fused ectopic lef from double mutnt, fused proximl to rrow.
3 Note 1695 Figure 2. td1-glf vegettive meristems re smller. (A) Height nd width (micrometers) of B73 (open tringles), B73/td1-glf (solid squres), nd td1-glf/td1-glf (shded dimonds) were mesured nd plotted. (B) Men heights, widths, nd rtios for ech genetic clss. Stndrd devitions re in prentheses. P-vlues for t-tests compring the clsses re lso shown. The lck of sttisticl difference in rtios for the three clsses indictes they re proportionl. B73 is sttisticlly similr to B73/td1-glf heterozygotes, indicting tht single td1- glf llele hs no ffect on vegettive meristem size. Plnts were grown in growth chmber with the following conditions: 16 hr of light t 26 ; 8 hr of drkness t 22. Vegettive meristems were mesured 14 dys fter sowing (DAS) fter dissection nd viewing under Nikon SMZ800 microscope. density on continuous meristemtic surfce (Figure 3B) (Bommert et l. 2005). Double-mutnt ers (Figure 3D) resembled those of kn1 plnts (Figure 3C), with ptches of rchis lcking spikelets nd similr spikelet TABLE 2 td1-glf increses the penetrnce of the kn1-e1 ectopic lef phenotype nd promotes fusion of ectopic leves in the B73 genetic bckground Genotype Ectopic leves b Penetrnce (%) F 2 fmily kn1/kn1; td1/td1 4 (2.5; 4) 100 kn1/kn1; td1/1 4 (0.7; 10) 40 kn1/kn1; 1/1 1 (0.2; 5) 20 kn1/1; td1/td1 0 (0; 13) 0 kn1/1; td1/1 0 (0; 19) 0 kn1/1; 1/1 0 (0; 19) 0 1/1; td1/td1 0 (0; 11) 0 1/1; td1/1 0 (0; 5) 0 1/1; 1/1 0 (0; 10) 0 1:1 fmily kn1/kn1; td1/td1 9 (1.90; 10) 90 (12/19) c kn1/1; td1/td1 8 (0.45; 20) 40 (2/9) td1-glf ws bckcrossed to B73 nine times nd the kn1-e1 llele ws bckcrossed to B73 six times. An F 1 plnt with these two prents ws self-pollinted. F 2 plnts were ssyed by PCR for ll possible llelic combintions nd double mutnt ws crossed with kn1-e1/1 td1-glf/ td1-glf plnt to generte fmily segregting 1:1 for kn1-e1 homozygotes in the td1-glf mutnt bckground. Plnts were grown under greenhouse conditions. density (Tble 3). However, insted of solid rchis, ectopic spikelets formed inside ers of double mutnts (Figure 3E) nd the rchis fused distlly, phenotype not observed in kn1 or td1 single-mutnt ers (dt not shown). Summry: STM nd CLV loci competitively regulte the blnce of centrl nd peripherl zones of the shoot picl meristem (Clrk et l. 1996). To ssess whether this reltionship exists in mize, we nlyzed the interction of td1 nd kn1. td1-glf does not suppress the limited shoot phenotype of kn1-e1, possibly becuse td1 vegettive meristems re smller. kn1-e1 suppresses the fscition of td1-glf inflorescences, indicting tht the bnorml growth of fscited meristems requires norml kn1 function. td1-glf fils to suppress the ectopic leves of kn1 mutnts; rther, it enhnces the phenotype. td1-glf increses fusion of these ectopic leves to their subtending leves, defect meliorted by norml kn1 lleles. In ddition, new phenotype ws seen in double mutnts: ectopic spikelets inside ers. Thus, KN1 nd TD1 function in liner pthwy mintining homeostsis in the vegettive meristem nd er, during spikelet initition. Becuse td1 mutnt ers re fscited yet their vegettive meristems re smller, the function Not significntly different from expected F 2 rtio (X 2, P. 0.05). b Number of plnts with ectopic leves followed by men number of ectopic leves per plnt nd smple size in prentheses. c Number of fused ectopic leves/totl number of ectopic leves.
4 1696 C. Lunde nd S. Hke nd KN1 lso converge to mintin cob identity nd lterl orgn initition. Like the BAM genes, td1 is widely expressed (Bommert et l. 2005) nd these multiple roles my be dependent upon tissue specificity of other pthwy members. We conclude tht the reltionship between td1 nd kn1 is not directly comprble to tht of CLV1 nd STM, std1, like the BAM genes, hs multiple functions throughout development. We thnk Rebecc Brt, Rchel Bond, Future Zhou, Ltici Holley, nd Ln M for their ssistnce in fieldwork, dt collection, nd nlysis. Members of the Hke lb provided helpful critique of the mnuscript. Dvid Hntz nd Julie Clfs provided excellent plnt cre. Funding for this project ws from Ntionl Science Foundtion DBI grnt (to S.H.). Figure 3. Reproductive phenotypes. Unpollinted ers of (A) norml sibling, (B), td1-glf homozygote, (C) kn1-e1 homozygote, nd (D) double mutnt. Ptches of cob hve filed to initite kernel primordi in the double mutnt, s seen in kn1- E1 homozygotes. (E) A longitudinl section of the sme er in D. Arrow in E points to ectopic kernel primordi in the er core, phenotype not seen in either single mutnt. of TD1 is similr to CLV1 in the inflorescence nd florl meristems, but more similr to BAM (DeYoung et l. 2006) in vegettive meristems. The synergism displyed by ectopic leves nd ectopic spikelets suggests tht TD1 TABLE 3 kn1-e1 is episttic to td1-glf in er spikelet formtion Genotype Er spikelets (n) A. Er spikelet counts 1/ ; 1/ (12.91; 31) td1/td1; 1/ (16.14; 23) 1/ ; kn1/kn (5.82; 11) td1/td1; kn1/kn (5.01; 6) Genotype P-vlues B. Comprisons of er spikelet counts of the td1-glf; kn1-e1 F 2 fmily td1/td1; 1/ vs. 1/ ; 1/ 0.002** 1/ ; kn1/kn1 vs. 1/ ; 1/ 0.000*** td1/td1; 1/ vs. 1/ ; kn1/kn *** td1/td1; kn1/kn1 vs. 1/ ; 1/ 0.001** td1/td1; kn1/kn1 vs. td1/td1; 1/ 0.000*** td1/td1; kn1/kn1 vs. 1/ ; kn1/kn Plnts from the td1-glf; kn1-e1 F 2 fmily were grown in the greenhouse nd observed. (A) Unpollinted er spikelet counts. Numbers re men vlues with stndrd devitions in prentheses followed by the number of plnts mesured. (B) P-vlues of two-tiled Student s t-test of er spikelet counts compring the genetic clsses. **Vlues re significnt t the 1% level; ***vlues re significnt t the 0.1% level. Numbers of spikelets were counted from cross section of the er t its widest point, 1 cm from the er tip. LITERATURE CITED Brton, M. K., nd R. S. Poethig, 1993 Formtion of the shoot picl meristem In Arbidopsis thlin: n nlysis of development in the wild type nd in the shoot meristemless mutnt. Development 119: Bhtt, A. M., J. P. Etchells, C. Cnles, A. Lgodienko nd H. D Ickinson, 2004 VAAMANA: BEL1-like homeodomin protein, intercts with KNOX proteins BP nd STM nd regultes inflorescence stem growth in Arbidopsis. Genes Dev. 328: Bommert,P.B.,C.Lunde,J.Nrdmnn,E.Vollbrecht,M.P.Running et l., 2005 thick tssel dwrf1 encodes puttive mize orthologue of the Arbidopsis CLAVATA1 leucine-rich receptor-like kinse. Development 132: Brnd, U., M. Grunewld, M. Hobe nd R. Simon, 2002 Regultion of CLV3 expression by two homeobox genes in Arbidopsis. Plnt Physiol. 129: Clrk, S.E., M. P. Running nd E. M. Meyerowitz, 1993 CLAVATA1, regultor of meristem nd flower development in Arbidopsis. Development 119: Clrk, S. E., M. P. Running nd E. M. Meyerowitz, 1995 CLAVATA3 is specificregultorof shoot ndflorlmeristemdevelopmentffecting the smeprocesses sclavata1. Development121: Clrk, S. E., S. E. Jcobsen, J.Z.Levin nd E. M. Meyerowitz, 1996 The CLAVATA nd SHOOT MERISTEMLESS loci competitively regulte meristem ctivity in Arbidopsis. Development 122: Clrk, S. E., R. W. Willims nd E. M. Meyerowitz, 1997 The CLAVATA1 gene encodes puttive receptor kinse tht controls shoot nd florl meristem size in Arbidopsis. Cell 89: DeYoung, B. J., K. L. Bickle, K. J. Schrge, P. Muskett, K. Ptel et l., 2006 The CLAVATA1-relted BAM1, BAM2 nd BAM3 receptor kinse-like proteins re required for meristem function in Arbidopsis. Plnt J. 45: DeYoung, B. J., nd S. E. Clrk, 2008 BAM receptors regulte stem cell specifiction nd orgn development through complex interctions with CLAVATA signling. Genetics 180: Endrizzi, K., B. Moussin, A. Hecker, J. Z. Levin nd T. Lux, 1996 The SHOOT MERISTEMLESS gene is required for mintennce of undifferentited cells in Arbidopsis shoot nd florl meristems nd cts t different regultory level thn the meristem genes WUSCHEL nd ZWILLE. Plnt J. 10: Fletcher, J. C., U. Brnd, M. P. Running, R. Simon nd E. M. Meyerowitz, 1999 Signling of cell fte decisions by CLAVATA3 in Arbidopsis meristems. Science 183: Jeong, S., A. E. Trotochud nd S. E. Clrk, 1999 The Arbidopsis CLAVATA2 gene encodes receptor-like protein required for the stbility of the CLAVATA1 receptor-like kinse. Plnt Cell 11: Knrr, S., O. Onguk nd H. M. Smith, 2006 Arbidopsis inflorescence rchitecture requires the ctivities of KNOX-BELL homeodomin heterodimers. Plnt 224: Kyes, J. M., nd S. E. Clrk, 1998 CLAVATA2, regultor of meristem nd orgn development in Arbidopsis. Development 125:
5 Note 1697 Kerstetter, R. A., D. Ludenci-Chingcunco, L.G.Smith nd S. Hke, 1997 Loss of function muttions in the mize homeobox gene, knotted1, re defective in shoot meristem mintennce. Development 124: Lenhrd, M., G. Jurgens nd T. Lux, 2002 The WUSHEL nd SHOOT MERISTEMLESS genes fulfill complementry roles in Arbidopsis shoot meristem regultion. Development 129: Leyser, H. M. O., nd I. J. Furner, 1992 Chrcteristion of three shoot picl meristem mutnts of Arbidopsis thlin. Development 116: Long, J. A., E. I. Mon, J.I.Medford nd M. K. Brton, 1996 A member of the KNOTTED clss of homeodomin proteins encoded by the SHOOTMERISTEMLESS gene of Arbidopsis. Nture 379: Ogw, M., H. Shinohr, Y. Skgmi nd Y. Mtsubyshi, 2008 Arbidopsis CLV3 peptide directly binds CLV1 ectodomin. Science 319: 294. Smith, L. G., B. Greene,B.Veit nd S. Hke, 1992 A dominnt muttion in the mize homeobox gene, Knotted-1, cuses its ectopic expression in lef cells with ltered ftes. Development 116: Suzki, T., M. Sto, M. Ashikri, M. Miyoshi, Y. Ngto et l., 2004 The gene FLORAL ORGAN NUMBER1 regultes florl meristem size in rice nd encodes leucine-rich repet receptor kinse orthologous to Arbidopsis CLAVATA1. Development 131: Suzki, T., T. Torib, M. Fujimoto, N. Tsutsumi, H. Kitno et l., 2006 Conservtion nd diversifiction of meristem mintennce mechnism in Oryz stiv: function of the FLORAL ORGAN NUMBER2 gene. Plnt Cell Physiol. 47: Suzki, T., A. Yoshid nd H. Hirno, 2008 Functionl diversifiction of CLAVATA3-relted CLE proteins in meristem mintennce in rice. Plnt Cell 20: Vollbrecht, E., L. Reiser nd S. Hke, 2000 Shoot meristem size is dependent on inbred bckground nd presence of the mize homeobox gene, knotted1. Development 127: Communicting editor: S. Venktesn
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