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Purple-leaved Ficus lyrata plants produced by overexpressing a grapevine VvMybA1 gene

Purple-leaved Ficus lyrata plants produced by overexpressing a grapevine VvMybA1 gene
Purple-leaved Ficus lyrata plants produced by overexpressing a grapevine VvMybA1 gene

ORIGINAL PAPER

Purple-leaved Ficus lyrata plants produced by overexpressing a grapevine VvMybA1gene

Jietang Zhao ?Zhijian T.Li ?Juan Chen ?

Richard J.Henny ?Dennis J.Gray ?Jianjun Chen

Received:27March 2013/Revised:18July 2013/Accepted:30July 2013/Published online:8August 2013óSpringer-Verlag Berlin Heidelberg 2013

Abstract

Key message This study established an ef?cient method of regenerating plants of Ficus lyrata and pro-ducing purple-leaved F.lyrata plants through genetic transformation using a VvMybA1gene of grapevine.Abstract Ficus lyrata ,a species with unique violin-or guitar-shaped leaves,was regenerated from leaf-derived calli cultured on Murashige and Skoog (MS)basal medium supplemented with 4.5l M N -phenyl-N’-1,2,3-thiadiazol-5-yl urea (TDZ)and 0.5l M a -naphthalene acetic acid (NAA).Leaf discs were inoculated with Agrobacterium tumefaciens strain EHA 105harboring a binary vector DEAT that contains the VvMybA1gene and neomycin phosphotransferase (npt II )gene and subsequently cultured on the established regeneration medium supplemented with 100mg l -1kanamycin.Results showed that 87.5%of the leaf discs produced kanamycin-resistant callus,and 68.8%of them produced adventitious shoots.Transgenic plants with three leaf colors including green,green-purple,and purple were produced.Regular and quantitative real-time PCR analyses con?rmed the integration of transgenes into the host genome.Semi-quantitative RT-PCR analysis indicated that the VvMybA1gene was responsible for the

purple-colored phenotype.Purple-leaved plants with strong color stability grew vigorously in a greenhouse.This study illustrated the feasibility of using a genetically engineered VvMybA1gene for drastic modi?cation of leaf color of an important woody ornamental plant.

Keywords Anthocyanin áFicus lyrata áFiddle leaf ?g áTDZ áVvMybA1

Introduction

The genus Ficus ,commonly known as ?g,is a member of the family Moraceae and composed of more than 800species.Figs are woody trees,shrubs,or vines native to the tropics of Africa,Asia,Australia,and Central and South America (Huxley 1992).Among cultivated species,F.carica has been grown for its edible fruit.Other species,such as F.benjamina ,F .elastica ,F .lyrata ,and F.pumila ,are produced for their ornamental value either as landscape plants in the tropics and subtropics or foliage plants used for interiorscaping (Henny and Chen 2003).Ornamental ?gs are among the top of listed potted foliage plants in the USA and valued for their differently shaped leaves that are either of dark green or brightly variegated (Chen et al.2005).With rapid expansion of the ornamental industry,there is an increasing demand for new ?g cultivars with leaves in different shapes or colors (Henny and Chen 2003;Fang et al.2007).

Fig improvement,thus far,has been focused on F.carica (Mars 2003);there are no breeding programs devoted to improving their ornamental value.New orna-mental ?g cultivars were primarily developed from a selection of either sports or somaclonal variants (Henny and Chen 2003;Fang et al.2007).Because somatic

Communicated by K.Kamo.

J.Zhao áZ.T.Li áR.J.Henny áD.J.Gray áJ.Chen (&)Mid-Florida Research and Education Center,University of Florida,Institute of Food and Agricultural Sciences,2725S.Binion Road,Apopka,FL 32703,USA e-mail:jjchen@u?.edu

J.Chen

Key Laboratory of Plant Resources Conservation and

Sustainable Utilization,the Chinese Academy of Sciences,No 723,Xingke Road,Tianhe District,Guangzhou 510650,China

Plant Cell Rep (2013)32:1783–1793DOI 10.1007/s00299-013-1491-5

mutations are random events and occur at a low frequency and often result in undesirable phenotypes,new cultivars developed through the selection of somatic mutations are limited(Chen and Henny2006).Genetic transformation offers a promising tool for introducing agronomically and economically important traits into known genotypes with-out altering the existing elite genetic background.Addi-tionally,new cultivar development through genetic engineering is ef?cient and can signi?cantly reduce the time normally required for traditional breeding.

Woody plants are considerably recalcitrant to genetic transformation due to dif?culty in regeneration(Giri et al. 2004).Techniques for micropropagating different Ficus species have been developed using shoot tips or axillary bud explants(Muriithi et al.1982;Pontikis and Melas 1986;Deshpande et al.1998;Kumar et al.1998),but in vitro culture of existing meristems is not a suitable approach for genetic transformation.Regeneration through callus has also been reported in Ficus,including F.lyrata, F.carica,and F.religiosa(Debergh and De Wael1977; Jaiswal and Narayan1985;Jona and Gribaudo1987;del Amo-Marco and Picazo-Gonzalez1992;Yakushiji et al. 2003;Kim et al.2007).Recently,regeneration and trans-formation of F.carica have been achieved(Yancheva et al. 2005;Soliman et al.2010).These studies,however,only utilized the b-glucuronidase(GUS)reporter gene,and the reported transformation frequencies were relatively low. To our knowledge,there has been no report on the use of agronomically and economically important genes for improving?g through genetic transformation.

Regardless of?owers or leaves,color is one of the most important traits in ornamental plants.Color and pigmen-tation patterns primarily result from biosynthesis of anthocyanins,carotenoids,and chlorophylls(Grotewold 2006).Anthocyanin pigments are derived from the?avo-noid biosynthetic pathway,and their biosynthesis has been well documented(Grotewold2006).Three major families of anthocyanin-regulatory gene products,R2R3MYB, basic helix-loop-helix(bHLH)transcription factors,and WD40protein,have been studied(Koes et al.2005).R2R3 MYB and bHLH transcription factors were identi?ed in a wide range of plant species(Hichri et al.2011).Constitu-tive expression of either R2R3MYB or bHLH genes in a heterologous system has been shown to be suf?cient to induce pigmentation caused by anthocyanin accumulation (Lloyd et al.1992;Mooney et al.1995;Geekiyanage et al. 2007;Li et al.2011,2012).

VvMybA1,a R2R3MYB-related gene from Vitis vinif-era,is known to regulate anthocyanin biosynthesis by controlling expression of the gene for UDP-glucose:?avo-noid3-O-glucosyltransferase(UFGT).The UFGT gene has been shown to be critical for anthocyanin biosynthesis in grapes(Kobayashi et al.2002).The VvMybA1gene is inactive in some white grape cultivars due to a retrotrans-poson insertion within the promoter sequence of VvMybA1 (Kobayashi et al.2004).Kobayashi et al.(2002)found that VvMybA1could induce UFGT gene expression and anthocyanin production in non-colored grape somatic embryos when transiently expressed.Recent studies dem-onstrated that stable ectopic expression of the VvMybA1 gene resulted in anthocyanin production in tobacco and grape(Li et al.2011,2012).Highly homogeneous antho-cyanin expression and high-intensity red to purple color in all parts of the engineered grapevine plants were observed (Li et al.2011).These?ndings provide a basis for manipulating pigment production in ornamental plants through the use of the VvMybA1gene.

The objectives of this study were to(1)develop a method for ef?cient regeneration of F.lyrata;(2)use the established method and Agrobacterium-mediated transfor-mation for producing transgenic plants with overexpression of the grape VvMybA1gene;and(3)select transgenic plants with different levels of anthocyanin accumulation for use in new cultivar development.

Materials and methods

Plant materials

In vitro culture of Ficus lyrata was initially established by Oglesby Plant International,Inc.(Altha,FL,USA)using shoot tips.Brie?y,microshoots were cultured in glass baby-food jars containing Murashige and Skoog(MS) (Murashige and Skoog1962),mineral salts and vitamins, 3%(w v-1)sucrose,and0.7%(w v-1)agar(Sigma,St. Louis,MO,USA)supplemented with8.8l M6-benzyl-aminopurine(BA).The cultures were maintained under a 16-h photoperiod with a photosynthetic photon?ux density (PPFD)of80l mol m-2s-1provided by cool-white?uo-rescent tubes and subcultured every4weeks.

Plant regeneration

Young leaves,approximately2cm wide and3cm long, were collected from the in vitro cultured plantlets and cut into1cm discs as explants for developing methods of regenerating F.lyrata.The following three treatments for optimizing callus induction and adventitious shoot regen-eration were evaluated:Leaf explants were initially cul-tured on MS basal medium supplemented with(1)4.4l M BA,(2) 4.0l M CPPU(N-(2-chloro-4-pyridyl)-N’-phe-nylurea),or(3)4.5l M TDZ(N-phenyl-N’-1,2,3-thia-diazol-5-yl urea),respectively.All treatments contained 0.5l M a-naphthalene acetic acid(NAA).There were eight explants per Petri dish,and four replicates per treatment.

Leaf discs were cultured in the dark at26°C for8weeks. Explants with callus were sub-cultured onto the same fresh medium and maintained at26°C under the PPFD of 80l mol m-2s-1with a16-h photoperiod for another 8weeks for adventitious shoot induction.Shoots were rooted in MS basal medium supplemented with0.5l M NAA.Callus initiation and adventitious shoot induction frequencies were calculated based on the number of explants with induced callus or shoots versus the total number of explants cultured per treatment.The particular medium resulting in the highest frequencies of both callus and shoot induction was used for genetic transformation.

Agrobacterium-mediated transformation

The Agrobacterium tumefaciens stain EHA105harboring the binary vector DEAT(Fig.1)was used for transforming F.lyrata with a grapevine VvMybA1gene.The DEAT vector contained the VvMybA1gene controlled by a dou-ble-enhanced CaMV35S promoter and an egfp/npt II fusion gene driven by a double-enhanced CsVMV promoter.The fusion gene was used for selection of transformants and monitoring their transformation status.Details about the vector have been described previously(Li et al.2011).

Agrobacterium cultures were initiated in a100ml?ask containing25ml of MG/L medium(Gar?nkle and Nester 1980)supplemented with100mg l-1kanamycin and 20mg l-1rifampicin and grown overnight at28°C on a rotary shaker at200rpm.Bacterial cells were harvested by centrifugation at5,000rpm for5min and then re-sus-pended in an equal volume of liquid regeneration medium (MS basal medium supplemented with4.5l M TDZ and 0.5l M NAA)containing100l M acetosyringone(AS). The resulting cell suspension culture was incubated for3h under the same conditions prior to use in transformation. Leaf discs of F.lyrata were submerged in bacterial solu-tion for10min,followed by removal of excessive liquid on sterile?lter paper.Infected leaf discs were then transferred onto?lter papers wetted with the liquid regeneration medium with100l M AS and co-cultivated in the dark at 26°C for3days.After co-cultivation,transient GFP expression in leaf discs was checked using a Leica MZFLIII stereomicroscope equipped with epi-?uorescence illumination and detection systems(Leica Microscopy System Ltd.,Heerbrugg,Switzerland).

Infected leaf discs were transferred onto solid regener-ation medium supplemented with200mg l-1of carbeni-cillin and cefotaxime,respectively,as well as100mg l-1 kanamycin.There were eight Petri dishes with six infected leaf discs per dish.The culture was maintained under the same conditions as described previously for plant regen-eration.After8weeks of culture in the dark,stable trans-formation frequency was estimated based on the number of explants producing a GFP-positive or red-colored callus versus the total number of co-cultivated explants.

For adventitious shoot induction,explants with kana-mycin-resistant callus were transferred onto the same medium and cultured for8weeks under light.A shoot induction frequency was calculated based on the number of explants with adventitious shoots versus the total number of co-cultivated explants.Kanamycin-resistant green and purple shoots were then transferred onto MS basal medium supplemented with0.5l M NAA and100mg l-1kana-mycin,as well as200mg l-1cefotaxime and carbenicillin, respectively,in baby-food jars for rooting and further plantlet growth.Plantlets with well-developed roots were transferred to a soilless substrate containing40%sphag-num peat,25%pine bark,25%coconut coir,and10% styrofoam by volume and grown in a shaded greenhouse with a PPDF of350l mol m-2s-1.

DNA extraction and PCR analysis

Genomic DNA was extracted from young leaves of the putative transgenic and wild-type plants as described by Owino et al.(2004).The presence of the egfp and VvMybA1genes in transgenic plants was detected by PCR analysis,where the EG-51(50-ATGGTGAGCAAGGGCG AGGAGCTGT-30)and EG-32(50-CTTGTACAGCTCGT CCATGCCGAGA-30)primers were used for amplifying a 717bp coding region of the egfp gene,and the MYB-51 (50-CCGCCACCATGGAGAGCTTAGGAGTTAGAAA-30) and MYB-32(50-ACTAGTTCAGATCAAGTGATTT ACTTGTGTG-30)primers were used for amplifying a959bp fragment of the VvMybA1coding region.The ampli?cation reactions consisted of1cycle at95°C for3min and40cycles at94°C for30s,55°C for40s,72°C for1min,followed by an extension cycle of8min at72°C.Plasmid DNA used in transformation served as a positive control,while DNA from non-transformed wild-type plants was used as a

negative Fig.1Schematic diagram of T-DNA region of the binary plasmid

DEAT.dCaMV35S double-enhanced(29-419to-90)CaMV35S

promoter with the X leader sequence of tobacco mosaic virus,

dCsVMV double-enhanced(29-443to-123)CsVMV promoter,

35S-30the termination site and polyadenylation signal of the CaMV

35S transcript,RB right border,LB left border

control.PCR products were analyzed by electrophoresis on 1.2%agarose gels.

Quantitative real-time PCR for the detection

of transgene copy number

The1C genome size of F.lyrata was calculated using the PARTEC PA cytometer(Partec GmbH,Mu¨nster,Ger-many)following the protocol described by Zhao et al. (2012).Transgene copy number(VvMybA1gene)in transgenic plants was determined using quantitative real-time PCR as previously described(Dutt et al.2008;Zhao et al.2013).Randomly selected two green-,two green-purple-,and three purple-leaved plants were analyzed. Quantitative real-time PCR was conducted in a Light-Cycler480òinstrument equipped with a96-well plate Therma-base and software release v1.5(Roche Molecular Biochemicals,Indianapolis,IN,USA).Samples were rep-licated three times,and the experiments were repeated twice.

Semi-quantitative RT-PCR analysis

Total RNA was isolated from randomly selected two plants per wild-type,transgenic green-,green-purple-,and purple-leaved plants using the modi?ed CTAB/NaCl method(Asif et al.2000).The RNA was treated with RQ1RNase-free DNase I(Promega,Madison,WI,USA)to avoid genomic DNA contamination.First-strand cDNA was synthesized from1l g of total RNA with oligo(dT)primer,using the ImProm-II TM Reverse Transcription System(Promega, Madison,WI,USA)based on the manufacturer’s protocol. The primers MYB-51and MYB-32were used for analyz-ing the expression of VvMybA1gene in transgenic plants. The Actin gene(Genbank No.KC841863)was ampli?ed using the primers ActinF(50-GTGTTGGATTCTGGTG ATGGT-30)and ActinR(50-CATATGCCAGCTTCT CCTTCA-30)as an internal control.The reaction included an initial3min of denaturation at95°C,followed by30s at94°C,40s at55°C,and1min at72°C with30cycles, plus a?nal10min extension at72°C.PCR products were separated electrophoretically on1.2%TAE-agarose gels with ethidium bromide and visualized under UV light. Analysis of anthocyanin content

Relative anthocyanin level was determined based on the method described by Neff and Chory(1998).The third leaf counting from the apical meristem was collected from the following groups of plants at an age of4months:(1)wild type,(2)transgenic with green leaves,(3)transgenic with green-purple leaves,and(4)transgenic with purple leaves grown in a shaded greenhouse.Frozen leaf tissue(1g fresh weight)was ground to powder and extracted in6ml of methanol acidi?ed with1%HCl overnight in a dark refrigerator.After the addition of4ml of distilled water, anthocyanins were separated from chlorophylls with equal volume of chloroform and were determined by measuring the A530and A657of the aqueous phase using a SmartSpec 3000spectrophotometer(BioRad,Hercules,CA,USA). The relative amount of anthocyanin per gram of fresh weight was calculated by subtracting the A657from the A530.

Statistical analysis

The data on the frequencies of callus and shoot induction as well as the relative amount of anthocyanin were analyzed using one-way ANOVA.When signi?cance occurred, mean differences were separated by Fisher’s protected least signi?cant differences(LSD)at P\0.05level.

Results

Plant regeneration through indirect shoot organogenesis An indirect shoot organogenesis procedure was established for the regeneration of F.lyrata.Results showed that the induction frequencies of both callus and adventitious shoots varied signi?cantly with the growth regulator combinations (Fig.2).TDZ with NAA induced signi?cantly more leaf explants to produce callus and more explants with adven-titious shoots.As a result,93.8%of the explants produced callus and78.1%developed adventitious shoots

compared

Fig.2Effect of the Murashige and Skoog basal medium supple-mented with BA,CPPU,or TDZ with NAA on the frequencies of callus induction and adventitious shoot formation of in vitro cultured leaf explants of F.lyrata.Error bars represent standard errors.Bars with different letters are signi?cantly different(P\0.05)based on Fisher’s protected least signi?cant difference

to62.5and3.1%,respectively,for BA with NAA or68.8 and18.8%,respectively,for CPPU with NAA(Fig.2). Thus,the MS basal medium containing4.5l M TDZ and 0.5l M NAA was used as the regeneration medium for genetic transformation.

Transformation and regeneration of plants from leaf explants

After co-cultivation of leaf explants with A.tumefaciens EHA105harboring DEAT for3days,strong transient GFP expression was detected at the cut edges of leaf explants(Fig.3a).The percentage of transient GFP-expressing explants was100%among leaf discs infected with Agrobacterium.Kanamycin-resistant callus appeared from co-cultivated leaf explants after4weeks of culture on regeneration medium in the dark.Callus proliferation took another4weeks before culture under light.Kanamycin-resistant callus exhibited variations in coloration(Fig.3b).Callus pieces transformed with VvMybA1gene were whitish-yellow,but some had red spots.Those red-spotted calli subsequently became red to purple in color,indicating increased anthocyanin accu-mulation in those callus pieces.

After transfer of cultures to light conditions,the kana-mycin-resistant callus developed numerous adventitious shoots.The whitish-yellow color calli produced green shoots on kanamycin-containing medium(Fig.3c).All kanamycin-resistant shoots exhibited stable GFP expres-sion(Fig.3d).Purple shoots were regenerated from purple callus(Fig.3e).The frequencies of co-cultivated explants producing callus and adventitious shoots were87.5and 68.8%,respectively.Regenerated kanamycin-resistant shoots were separated based on green or purple color when they were about2cm in height and transferred onto rooting medium in baby-food jars for rooting.The rooting per-centages of transferred shoots were100%.

Anthocyanin accumulation in regenerated plants

A total of103kanamycin-resistant shoots were recovered (Table1).Five of them had purple-colored shoots;they also produced purple-colored roots(Fig.3e)and subse-quently the entire plants became purplish(Fig.3f).The remaining98plantlets had green shoots:27produced red roots(Fig.3g)and71white roots after they were cul-tured in rooting medium.All transgenic plantlets were transplanted to a soilless substrate and grown in the greenhouse.Both purple and green plants grew vigor-ously(Fig.3h,i).

After4months of growth in the greenhouse,plant height reached about40cm and plant phenotypes were evaluated.Plantlets that initially produced green shoots and white roots developed into green-leaved plants(Table1). Among the27plantlets that had green shoots but red roots, 24became green-leaved plants,two became green-purple-leaved plants,and one became a purple plant in the greenhouse.Of the two green-purple-leaved plants,one had whitish roots and the other had light purplish roots.The ?ve initially purplish plantlets remained purple in the greenhouse.Thus,a total of six purple plants were obtained.

PCR and quantitative real-time PCR analysis

PCR analysis of ten randomly selected transgenic plants including green-,green-purple-,and purple-leaved ones,as well as the wild type showed two bands at717and959bp. These bands corresponded to the egfp and VvMybA1genes, respectively and were absent in the wild-type plant(Fig.4a,b).

The1C genome size of F.lyrata estimated by the PARTEC PA cytometer was 6.169108bp.The copy number in transgenic plants was determined using quanti-tative real-time PCR.Extrapolated crossing pints(Cp) values from transgenic plants showed that the two green plants had three copies and the two green-purple and three purple plants had a single copy of the VvMybA1gene (Table2).Melting curve analysis of real-time PCR prod-ucts revealed that all the plasmid copy controls and trans-genic plants produced a single-peak pro?le,indicating that ?uorescence signals were derived from target-speci?c ampli?cation.

Anthocyanin quanti?cation and VvMybA1gene expression analysis

The third leaf of wild-type,and transgenic green,green-purple,and purple plants(Fig.5a)was used for analyzing anthocyanin content in relation to the purple coloration. The color intensities of the solutions extracted from wild-type and transgenic green-leaved plants were similar,but increasingly enhanced in transgenic green-purple-and purple-leaved plants(Fig.5b).Quantitative analysis showed that there was little change in anthocyanin content between the wild-type plant and transgenic green plant. However,signi?cantly higher anthocyanin contents were detected in transgenic green-purple-and purple-leaved plants.The relative anthocyanin contents in green-purple and purple leaves were,respectively,16and20times greater than the control plant(Fig.5c).

Semi-quantitative RT-PCR analysis of randomly selec-ted wild-type,transgenic green-,green-purple-,and purple-leaved plants showed the presence of an expected959bp transcript in all the transgenic plants,but absent in the wild type(Fig.6).Of the transgenic plants investigated,the highest level of VvMybA1expression occurred in purple-

Fig.3Regeneration of transgenic F.lyrata plants.a Transient GFP expression in leaf discs,b kanamycin-resistant callus in green or purple,c kanamycin-resistant green buds,d kanamycin-resistant green buds exhibited GFP expression,e the purple callus regenerated purple buds,f the plants with purple leaves and red roots,g the plants with green leaves and red roots,and h purple-and i green-leaved plants grew vigorously in the greenhouse

Table 1Transgenic Ficus lyrata plants differing in anthocyanin accumulation during in vitro culture and after being grown in a greenhouse for 4months

Cultural conditions Green plants Green plants with red roots Green-purple plants Purple plants In vitro 712705Greenhouse

95

2

6

Fig.4PCR analysis showing the presence of egfp (a )and VvMybA1(b )genes in the transgenic F .lyrata plants.M 1kb marker,WT wild-type plant control,1–10randomly selected transgenic plants

Table 2Copy numbers of VvMybA1gene in transgenic Ficus lyrata plants estimated by quantitative real-time PCR analysis

a

Mean values of crossing pints (Cp)from three replicates

b

Standard deviation values for Cp c

Mean values of extrapolated relative to a single transgene copy

Sample name Mean Cp a STD Cp b Mean conc c STD conc Copy number Plasmid-1copy 24.4830.1260.9880.0261Plasmid-2copies 22.2330.032 2.1490.0632Plasmid-3copies 21.8690.165 3.0220.0443Plasmid-4copies 21.6200.041 3.7600.1374Plasmid-5copies 21.3100.014 5.0050.0495Green plant-1

21.8360.051 3.0930.1423Green plant-221.8870.048 2.9530.1293Green-purple plant-124.6210.047 1.0220.0151Green-purple plant-224.0410.0390.9350.0001Purple plant-124.8750.013 1.1220.0061Purple plant-224.7990.043 1.0880.0181Purple plant-3

24.620

0.038

1.022

0.012

1

leaved plants,followed by green-purple-leaved plants.The lowest expression was in those green-leaved plants (Fig.6).

Discussion

Genetic transformation technologies have been used for modi?cation of a wide range of crops including ?eld crops,vegetables,and ornamentals (Chandler and Sanchez 2012).However,the use of such technologies for substantially improving the esthetic value of ornamental,particularly woody ornamental plants is rather limited (Chandler and Sanchez 2012).In the present study,we successfully regenerated transgenic F.lyrata plants with enhanced anthocyanin content in leaves by overexpressing the VvMybA1gene derived from V.vinifera ,from which six plants with stable,purple-colored leaves were obtained.The purple-leaved plants grew vigorously in the green-house.In addition to the difference in coloration,no other morphological differences were observed since August,2012.The purple-colored,violin-shaped leaves make them a sought-after novel plant.To our knowledge,this is the ?rst report of regeneration of transgenic Ficus species with an improved ornamental trait.

A reliable regeneration protocol is critically important for successful transformation.The present study estab-lished a highly ef?cient system for callus and adventitious shoot induction,with the respective frequency at 93.8and 78.1%,from leaf explants.This established method is simple and convenient as callus appeared from leaf explants cultured in the dark on MS basal medium con-taining 4.5l M TDZ and 0.5l M NAA,and adventitious shoots were regenerated from callus when explants with callus were cultured on the same fresh medium under lighting conditions.Our results indicated that TDZ was the most effective cytokinin in combination with NAA for regeneration of F.lyrata .Other reports also suggested

that

Fig.6Semi-quantitative RT-PCR analysis of VvMybA1gene in transgenic plants.WT wild-type plant,G green -leaved,G-P green-purple -leaved,and P purple -leaved transgenic plants.Actin1as an internal control

Fig.5Variation in anthocyanin accumulation in greenhouse-grown transgenic plants.a The third leaf of wild-type (WT )and transgenic green (G )-,green-purple (G-P )-,and purple (P )-leaved plants,b extracted solutions from the four leaves,c relative anthocyanin content of four leaves.Error bars represent SE.Bars with different letters are signi?cantly different (P \0.05)based on Fisher’s protected least signi?cant difference

b

TDZ with different auxins was effective in inducing adventitious shoots in Ficus species(del Amo-Marco and Picazo-Gonzalez1992;Yakushiji et al.2003;Yancheva et al.2005;Soliman et al.2010).For example,Kim et al. (2007)reported that TDZ with indole-3-butyric acid(IBA) could enhance multiple shoot induction and plant regen-eration from leaf segments of F.lyrata.TDZ is highly stable and resistant to degradation by cytokine oxidase (Mok et al.1987)and can also elicit both auxin and cytokinin responses(Gill and Saxena1993),which may partially explain why TDZ is more effective in inducing callus and adventitious shoots in Ficus species.

The established protocol is also ef?cient for genetic transformation.The frequencies of co-cultivated leaf discs producing callus and subsequently adventitious shoots were up to87.5and68.8%,respectively.A total of103 kanamycin-resistant plantlets were regenerated,and all of them were transgene positive,suggesting that there was no escape of non-transformants from kanamycin selection at 100mg l-1.This transformation ef?ciency is markedly higher compared to that of F.carica where only7.46%of the regenerants were GUS positive under50mg l-1 kanamycin selection(Yancheva et al.2005).Thus,a stringent condition of100mg l-1kanamycin is suggested here for regeneration and selection of transgenic Ficus species.

The present study shows that ectopic expression of the anthocyanin-regulatory gene VvMybA1in a non-host, F.lyrata,signi?cantly enhanced anthocyanin accumula-tion,resulting in purple pigmentation at the whole plant level.In previous transformation studies,overexpression of VvMybA1gene in grapevine resulted in purple pigmenta-tion in all parts of the plant;whereas VvMybA1overex-pression only produced several patches of purple spots in greenhouse-grown transgenic tobacco plants(Li et al. 2011).A similar anthocyanin expression pattern was also reported in transgenic tobacco expressing a VlmybA2gene, a homolog of VvMybA1(Geekiyanage et al.2007).How-ever,Mooney et al.(1995)reported that the expression of delila(del),a regulatory gene of Antirrhinum,induced different anthocyanin pigmentation in Arabidopsis, tobacco,and tomato.No abnormal phenotypes or restricted pigmentation were observed in Arabidopsis and tobacco, whereas pigmentation in vegetative tissue of tomato plants strongly increased(Mooney et al.1995).In addition, anthocyanin expression in maize is known to be dependent on both the R2R3MYB and bHLH types of transcription factors(Cone et al.1993).Expression of both Lc and Pl genes resulted in transgenic creeping bentgrass(Agrostis stolonifera L.)that was entirely purple;whereas expression of either Lc or Pl alone was not suf?cient to produce pigmentation in leaf cells(Han et al.2009).These results indicate that the induction of anthocyanin pigmentation in heterologous hosts could be signi?cantly affected by the speci?c transcription factor used and also the host plant species.

Our results showed that transformed callus and regen-erated plantlets exhibited variation in coloration(Fig.3). Some green shoots produced red roots,while the others developed white roots.Two transgenic plantlets with green shoots but red roots became green-purple-leaved plants in the greenhouse,and one plantlet with green shoots and red roots even became a completely purple-leaved plant when grown in the greenhouse.Since these plants were not purple at the callus and adventitious shoot stages,it was likely that this color variation could be related to tissue-speci?c and/or developmental-regulated expression of endogenous anthocyanin biosynthetic genes(Lloyd et al. 1992;Mooney et al.1995;Bradley et al.1998;Ray et al. 2003).However,the effects of greenhouse environments cannot be ruled out.Red-purple anthocyanin was observed in Lc transgenic alfalfa grown under either high light intensity or low temperature(Ray et al.2003),and intense purple anthocyanin pigmentation appeared only in Lc transgenic petunia grown under high light,but not under shade conditions(Albert et al.2009).

Three types of transgenic plants were obtained in accordance with the leaf coloration:green,green-purple, and purple(Fig.5a).The intensity of leaf coloration cor-responded to the relative anthocyanin contents of leaf tis-sues(Fig.5b,c).Semi-quantitative RT-PCR analysis revealed that the level of VvMybA1gene expression posi-tively corresponds to the degree of coloration among these transgenic plant types.Thus,the differences in anthocyanin accumulation re?ected different levels of VvMybA1gene expression.The transgene copy number analysis showed that there were three copies in two green-leaved plants,but the green-purple or purple plants had one copy(Table2). The low level of VvMybA1expression and correspondingly no purple coloration in the transgenic green-leaved plants were probably attributed to the increased copy numbers of the VvMybA1gene.This observation is consistent with previous?ndings that multiple transgene copies frequently lead to co-suppression and gene silencing(Vaucheret et al. 1998).However,the correlation between transgene copy number and gene expression level is known to be complex. Han et al.(2009)studied the in?uence of increased copy number on the expression level of Lc?Pl in creeping bentgrass and found that the expression level was inde-pendent of gene copy number.

Nevertheless,anthocyanins represent the major pig-ments in plants.Although there is increasing research effort on engineering of anthocyanin biosynthesis(Petroni and Tonelli2011),little research has focused on the manipu-lation of anthocyanin synthesis in ornamental foliage plants (Li et al.2005;Han et al.2009)despite the fact that the

wholesale value of foliage plant in2011was$613million in the USA(USDA2012).Thus far,the purple-leaved F. lyrata plants have been propagated through stem cutting and micropropagation.Subsequent production of the propagules in greenhouses showed that the purple trait has been stable and attractive.Other research efforts include the induced mutation of purple-leaved plantlets for poten-tial development of new cultivars from regenerated popu-lations(Chen and Henny2006).The success in manipulation of this gene in F.lyrata may suggest that the VvMybA1gene could be used for regulating anthocyanin biosynthesis in other ornamental plants,thus improving their esthetic and commercial value.

Acknowledgments The authors thank Oglesby Plant International, Inc.(Altha,FL,USA)for providing microshoots of Ficus lyrata and Terri Mellich for performing DNA?ow cytometry analysis. References

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