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PAPER

PUBLICATION

148 S. Kamala and T. Makeshkumar

Transgenic Elephant Foot Yam (Amorphophalluspaeoniifolius (Dennst.) Nicolson) Expressingβ-glucuronidase Reporter Gene

S. Kamala and T. Makeshkumar

Central Tuber Crops Research Institute, Sreekariyam, Thiruvananthapuram 695 017, Kerala, India

Corresponding author: T. Makeshkumar, e-mail: makeshctcri@gmail.com

Received: 24 August 2013; Accepted: 31 December 2013

AbstractElephant foot yam (Amorphophallus paeoniifolius (Dennst.) Nicolson) is infected by various diseasessuch as mosaic, collar rot and dry rot disease, which cause severe yield reduction. Disease resistancecan be achieved in crop plants through transgenic strategies. The present study is focused onAgrobacterium mediated transformation of A. paeoniifolius using β-glucuronidase (GUS) reporter gene.Friable callus cultures were established from corm lateral buds of A. paeoniifolius on modified Murashigeand Skoog (MS) medium supplemented with 0.5 mg l-1 each of 6-Benzyl aminopurine, 2,4-Dichlorophenoxy acetic acid and α- Naphthalene acetic acid. Friable callus and swollen petiole explants wereinfected with Agrobacterium tumefaciens strain AGLO harbouring the Ti vector pOYE 153 having uidAgene encoding GUS. The transformation event was confirmed by GUS histochemical analysis and lateron the presence of uidA gene was determined by Polymerase Chain Reaction (PCR). The highesttransformation efficiency of 36.37% was observed for callus when compared to swollen petiole explant.The presence of acetosyringone improved the transformation efficiency by 20 fold irrespective of theexplant. The present study serves as an initial step towards the development of transgenic A. paeoniifoliusfor disease resistance.

Key words: β-glucuronidase, acetosyringone, elephant foot yam, friable callus, in vitro, transformation

Introduction

Elephant foot yam (Amorphophallus paeoniifolius(Dennst.) Nicolson) is a tropical tuber crop belongingto the Araceae family. It is an economically importantcrop due to its production potential and popularity as avegetable. The corms and pseudostems of elephant footyam are popularly used in the preparation of indigenousayurvedic medicines (Misra et al., 2002). The tubers aredigestive, appetizer, anodyne, anti-inflammator y,astringent, haemostatic, rejuvenating and tonic in nature.They are used in the treatment of tumors, elephantiasis,inflammations, cough, asthma, constipation, fatigue andanaemia (Nair, 1993). In India, the plant is widelycultivated in Kerala, Tamil Nadu, Punjab, Assam, Biharand West Bengal. The crop is mainly cultivated in the

month of September-October, due to its high price andhence the crop is considered to be a cash crop due tohigh mean net profit. The plant is also cultivated as anintercrop with banana, turmeric and coconut (Ravi etal., 2009). In Kerala, this crop is cultivated in large areasin Ernakulam, Wayanad, Thrissur, Pathanamthitta andKozhikode (Ravindran and George, 2008).

Elephant foot yam is subjected to a variety of infectionssuch as mosaic disease caused by Dasheen mosaic virus(DsMV), collar rot caused by the fungus Sclerotiumrolfsii, dry rot disease caused by Fusarium solani andRhizoctonia solani. Among the diseases, mosaic diseasecaused by DsMV is the major yield constraint (Nehalkhanet al., 2006). Considering the importance of elephantfoot yam and the diseases presenting serious constraints

Journal of Root Crops, 2013, Vol. 39 No. 2, pp. 148-153Indian Society for Root CropsISSN 0378-2409

149Transgenic elephant foot yam

to the production of this crop, resistance developmentbecomes a high priority goal. As an initial step towardsdeveloping resistance in A. paeoniifolius throughtransgenic approach, an efficient callus multiplication aswell as transformation protocol has to be established.The process of in vitro regeneration of A. paeoniifoliusis far from being routine due to its recalcitrant nature(Mukherjee et al., 2009). Ban et al. (2009) developedresistance to soft rot disease in A. konjac usingAgrobacterium mediated transformation. The uidA geneof Escherichia coli encoding β-glucuronidase (GUS) hasbeen utilised in numerous plant species as a reportergene to confirm transformation (Jefferson et al., 1987;Wijayanto and McHughen, 1999; Basu et al., 2004).Upon integration into genome, GUS leads to bluecolouration upon simple biochemical analysis. Hence theobjective of the present study was the establishment ofin vitro callus cultures of A. paeoniifolius and theirsubsequent use as transformation explant source forAgrobacterium mediated transformation using GUSgene.

Materials and Methods

Plant material

The mother plants of A. paeoniifolius cv. Gajendra(Fig. 1a) were grown in open field of Central Tuber CropsResearch Institute (CTCRI), Thiruvananthapuram,Kerala, India. Lateral buds of corms and petioles wereused as explants.

Establishment of aseptic callus cultures

Lateral buds of field grown corms of A. paeoniifoliuswere surface sterilized with 0.1% (w/v) HgCl

2 for 1 min

followed by 70% (v/v) ethanol for 1 min. The petioleexplants were surface sterilized with 0.1% (w/v) Bavistinfor 60 min followed by 70% (v/v) ethanol for 1 min and0.1% HgCl

2 (w/v) for 7 min. Each treatment was followed

by washing thrice with sterile distilled water. As analternative, one step surface sterilization procedure byflaming the unopened leaves covered by cataphylls withabsolute alcohol was done to get petiole explants. Themethod proved to be effective in getting contaminationfree cultures, thus avoiding long steps of surfacesterilisation of petiole explants.

The explants were inoculated on modified Murashigeand Skoog (MS) medium (Murashige and Skoog, 1962)

supplemented with various combinations of 6-Benzylaminopurine (BA), 2,4-Dichloro phenoxy aceticacid (2,4-D) and α-Naphthalene acetic acid (NAA). Allcomponents of the medium including 3% sucrose andhormones were mixed and adjusted to pH 5.6 and 0.7%plant agar was added for solidifying the media. Thecultures were incubated under light intensity of 2500lux and temperature of 25 ± 2°C with 16 h light/8 hdark cycle.

Bacterial strain and media

The culture of Agrobacterium tumefaciens strain AGLOharbouring the plant transformation plasmid pOYE 153having uidA gene conferring GUS activity and npt IImarker maintained in the Transgenic Laboratory ofCTCRI was used for the transformation. A. tumefacienswas cultured in YEB medium (Beef extract - 3 g l-1, caseinhydrolysate - 5 g l-1, bacto yeast extract - 1 g l-1, sucrose- 5 g l-1, pH 7.5) containing MgSO

4 (2 mM) and

kanamycin (100 mg l-1). The strain was allowed to growin two sets of media one with acetosyringone (200 µM)and the other without acetosyringone at 28oC.

Preparation of Agrobacterium for transformation

The cultures of A. tumefaciens having pOYE 153(OD

600=1.0) were centrifuged at 5000 rpm for 10 min.

and the pellet was washed twice in liquid MS followedby suspension in the same volume of liquid MS.

Agrobacterium mediated transformation

Friable callus as well as swollen petiole explants was co-cultured in a petridish containing A. tumefaciens cultureand shaken for 30 min. and 60 min. respectively. Theexplants were dried on a filter paper. The explants wereco-cultivated on callus induction (CI) medium with andwithout acetosyringone. After 4 days of co-cultivationat 22oC in the dark, the explants were washed thricewith sterile distilled water followed by liquid MS mediumwith ticarcillin (500 mg l-1) twice. Then the explantswere allowed to grow on selection medium (CI with 500mg l-1 ticarcillin and 15 mg l-1 geneticin).

GUS assay and molecular analysis

GUS assay (Jefferson et al., 1987) was done to confirmthe transformation event. GUS buffer was prepared with50 mM Na

2HPO

4, 1 mM Na

2EDTA, 1 mM Fe+++/

Fe++CN and 0.1% Triton X-100. The pH was adjusted

150 S. Kamala and T. Makeshkumar

to 7.0 with NaOH, filter sterilised and kept in ambercoloured bottles at 4oC. The stock solution of 25 mg ml-1

5-bromo-4-chloro-3 indolyl-β-D-glucuronic acid (X-Gluc) was prepared in dimethyl sulfoxide and was storedat -20oC. The GUS assay buffer was prepared freshly bymixing 1 part of X-Gluc with 49 parts of GUS buffer.The explants were incubated overnight in GUS assaybuffer at 370C and were washed with 70% ethanol.

The putative transgenic callus and swollen petioleexplants of A. paeoniifolius found free fromAgrobacterium after four subsequent subcultures inticarcillin containing selection medium were used forDNA isolation with Spectrum DNA isolation kit (Sigma).The DNA was amplified with GUS specific primers(GUS-F 5’-GGGCATTCAGTCTGGATC-3’ and GUS-R 5’-GTGCGGATTCACCACTTG-3’) by incubating at94°C for 2 min followed by 35 cycles of 94°C for 30sec, 56°C for 1 min and 72°C for 1 min and a finalextension of 72°C for 10 min. The reaction mixture forthe amplification contained 5 ng µl-1 DNA, 1X PCRbuffer, 0.5 mM dNTP mix, 0.5 pmol µl-1 each of forwardand reverse primer, 0.05 U µl-1 Taq DNA Polymerase.The vector plasmid was used as positive control, whereasthe DNA isolated from untransformed callus was usedas negative control. Amplified PCR products wereelectrophoresed on 1.0% agarose gel with ethidiumbromide and visualized under ultraviolet (UV) light.Transformation efficiency was determined by dividingthe total number of PCR positive explants by the numberof explants inoculated and then multiplied by 100.

Results and Discussion

Induction and multiplication of callus cultures

Initially, lateral bud explants sprouted (Fig. 1b), whilethe petiole explants enlarged enormously (Fig. 1c).Whitish, yellowish white or pink friable callus (Fig. 1d)was initiated within 15-30 days of inoculation fromlateral bud and petiole on modified MS mediumsupplemented with 0.5 mg l-1 each of BA, 2,4-D andNAA (CI medium). The days to callusing and the callusing% differed significantly depending on the explant type(Table 1). MS medium with BA, 2,4-D or NAA alonewas not effective in inducing callus. The effectiveness ofusing two or more growth regulators in callus inductionhas been supported by previous studies on other plantspecies like A. campanulatus var. hortensis Backer(Irawati et al., 1986), Gerbera jamesonii (Aswath andChoudhary, 2002) and A. albus (Hu and Liu, 2008).

Transformation, GUS assay and molecular analysis

Transformed callus as well as swollen petiole explantswas selected based on its survival on antibiotic selectionmedium. Agrobacterium has been successfully utilisedhere for genetic transformation and has been reportedin many monocotyledon species like rice (Hiei et al.,1994), wheat (Cheng et al., 1997; Sahrawat et al., 2003),maize (Frame et al., 2002) and rye (Popelka and Altpeter,2003). GUS assay proved to be effective in confirmingthe transformation event within a short period aftertransformation (Table 2). The GUS assay of transformedexplants (swollen petiole and callus) showed positive blue

Table 1. Effect of growth regulators on callus induction in A. paeoniifolius

Growth regulators (mg l-1) Days to callus induction Callusing (%)

BA NAA 2,4-D Lateral bud Petiole Lateral Bud Petiole

0.0 0.0 0.0 0 0 0 00.5 0.0 0.0 0 0 0 00.0 0.5 0.0 0 0 0 00.0 0.0 0.5 25.43 ± 0.24 0 56 00.5 0.5 0.0 21.52 ± 0.19 29.00 ± 0.32 72 400.5 0.0 0.5 25.46 ± 0.24 0 52 00.0 0.5 0.5 25.84 ± 0.15 0 52 00.5 0.5 0.5 13.91 ± 0.18 15.56 ± 0.27 88 72

151Transgenic elephant foot yam

colour irrespective of the type of explants. Foreffective GUS sector observation and photography,TS View Version 7.3.1.7. was utilised (Figs. 2a and2b). Comparative analysis of transformationefficiency as influenced by explant type andacetosyringone is given in Table 2. The presence ofacetosyringone was found to increase thetransformation efficiency by 20 fold. Early reportsalso support the fact of transformation enhancingeffect of acetosyringone (Sheikholeslam and Weeks,1987; Suma et al., 2008). The callus was found to bemore suitable for transformation due to its ease ofregeneration as well as high transformation efficiencyof 36.67%. Ban et al. (2009) also used callus culturesof A. konjac for Agrobacterium mediatedtransformation for soft rot disease resistancedevelopment. After 4 weeks of incubation in selectionmedium, the transformed callus showed good growth,while the untransformed underwent browningwithout any further growth (Fig. 2c). PCRamplification of transgenic callus with GUS specific

Fig.2. a. Transformed and untransformed callus as distinguished by GUS assay; b. Transformed swollen petiole showing bluecolouration against untransformed explant on histochemical analysis; c. Transformed callus showing growth on selectionmedium Bars = 2mm

Table 2. Effect of explants and acetosyringone on transformation efficiency in A. paeoniifoliusExplants Acetosyringone Number of Number of Number of Number of Transformation

(µM) explants GUS blue PCR efficiencyinoculated positive sectors per positive (%)(~0.5 cm2) explants explant explants

Callus 0 30 5 1-10 4 13.33200 30 14 5-25 11 36.67

Petiole 0 30 2 1-5 1 03.33200 30 9 1-15 7 23.33

Fig.1. a. A. paeoniifolius; b. Sprouted lateral bud explant;c. Swollen petiole; d. Friable callus

152 S. Kamala and T. Makeshkumar

primers, which survived in the selection medium gave a band at 400bp, while the non transformed control callus failed to giveamplification (Fig. 3).

An in vitro callus multiplication as well as transformation protocolfor A. paeoniifolius has been established. This paper is first of itstype to report on Agrobacterium mediated transformation in A.paeoniifolius. It is expected that the present study may serve as aninitial step towards the development of virus resistant variety andfor other genetic modification with useful traits in A. paeoniifoliususing transgenic approach. GUS gene proved to be an effectivereporter gene in A. paeoniifolius. In vitro propagation of A.paeoniifolius as well as disease resistance development and their fieldrelease would greatly increase the availability of quality plantingmaterial.

Acknowledgement

The authors are grateful to the Director, CTCRI, for extending allthe facilities to carry out the work and the Council for Scientificand Industrial Research (CSIR) for providing Junior ResearchFellowship to the first author.

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