Abstract
Poly(ADP-ribose) polymerases (PARP) are involved in the regulation of plant growth and development, especially under stress conditions. These enzymes post-translationally modify target proteins by adding ADP-ribose polymers. This study presents the effect of PARP chemical inhibitor 3-methoxybenzamide (3 MB) on in vitro plant growth, microtuber formation, and Agrobacterium-mediated transformation of blue potato (Solanum tuberosum L. subsp. andigenum). The addition of 3 MB (0.2 to 0.6 mM) significantly increased the growth and microtuber formation of in vitro propagated plants. The highest gain in plant fresh weight, root mass, and microtuberization was observed in clonal propagation medium with 0.4 mM 3 MB. Transformation frequency of blue potato internodes increased to 43%, 2.7-fold over the non-treated control (16%), when 0.2 mM 3 MB was included in the culture medium during the whole process. The addition of 3 MB during Agrobacterium transformation did not affect transgene copy number in regenerated plants. Southern blot analyses and histochemical staining for ß-glucuronidase activity confirmed the presence and expression, respectively, of the uidA transgene in plant tissues. From these results, it can be concluded that the inhibition of PARP activity can increase biomass production and transformation rates for genetic improvement of blue potato.
Similar content being viewed by others
References
Ahlfors R, Lang S, Overmyer K, Jaspers P, Brosche M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, Inze D, Palva T, Kangasjarvi J (2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–1937
Altpeter F, Springer NM, Bartley L, Blechl AE, Brutnell TP, Citovsky V, Conrad LJ, Gervin SB, Jackson DP, Kausch AP, Lemaux PG, Medford JI, Orozco-Cárdenas ML, Tricoli DM, Van Eck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart N (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520
Amor Y, Babiychuk E, Inzé D, Levine A (1998) The involvement of poly (ADP-ribose) polymerase in the oxidative stress responses in plants. FEBS Lett 440:1–7
Banerjee AK, Prat S, Hannapel DJ (2006) Efficient production of transgenic potato (S. tuberosum L. ssp. andigena) plants via Agrobacterium tumefaciens- mediated transformation. Plant Sci 170:732–738
Briggs AG, Bent A (2011) Poly(ADP-ribosyl)ation in plants. Trends Plant Sci 16:372–380
Chen P-Y, Wang C-K, Soong S-C, To K-Y (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breed 11:287–293
Chetty VJ, Ceballos N, García D, Narváez-Vásquez J, López W, Orozco-Cárdenas ML (2013) Evaluation of four Agrobacterium tumefaciens strains for the genetic transformation of tomato (Solanum lycopersicum L.) cultivar micro-tom. Plant Cell Rep 32:239–247
Chetty VJ, Narváez-Vásquez J, Orozco-Cárdenas ML (2015) Potato (Solanum tuberosum L.). In: Wang K (ed) Methods in Mol. Biol. Agrobacterium protocols Springer. Human Press, NY, pp 85–96
De Block M (2000) Genetic transformation using a PARP inhibitor. US patent WO 6074876
De Block M, Verduyn C, Brouwer D, Cornelissen M (2005) Poly (ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95–106
Den BB (2010) High oil contents plants. US patent WO 2010142424A1
Ding R, Pommier Y, Kang VH, Smulson M (1992) Depletion of poly (ADP ribose) polymerases by antisense RNA expression results in a delay in DNA strand rejoining. J Biol Chem 267:12804–12812
Donnelli D, Coleman WK, Coleman SH (2003) Potato microtuber performance and production: a review. Am J Potato Res 80:103–115
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158
Hansen G (2000) Evidence for Agrobacterium-induced apoptosis in maize. Mol Plant Microbe Interact 13:649–657
Hussain I, Chaudhry Z, Muhammad A, Asghar R, Naqvi SMS, Rashid H (2006) Effect of chlorocholine chloride, sucrose, and BAP on in vitro tuberization in potato (Solanum tuberosum L. cv. Cardinal). Pak J Bot 38:275–282
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3909
Khanna HK, Paul JY, Harding RM, Dickman MB, Dale JL (2007) Inhibition of Agrobacterium-induced cell death by antiapoptotic gene expression leads to very high transformation efficiency of banana. Mol Plant Microbe Interact 20:1048–1054
Lachman J, Hamaouz K (2005) Red and purple potatoes as a significant antioxidant source in human nutrition – a review. Plant Soil Environ 51:477–482
Lamb RS, Citarelli M, Teotia S (2012) Functions of the poly (ADP-ribose) polymerase superfamily in plants. Cell Mol Life Sci 69:175–189
Liu C, Wu Q, Liu W, Gu Z, Wang W, Xu P, Ma H, Ge X (2017) Poly (ADP-ribose) polymerase regulates cell division and development in Arabidopsis roots. J Int Plant Biol 59:459–47411
Murashige T, Skoog FA (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497
Narváez-Vásquez J, Ryan AC (2002) The systemin precursor gene regulates both defensive and developmental genes in Solanum tuberosum. Proc Natl Acad Sci 99:15818–15821
Pruski K, Astatkie T, Nowak J (2002) Jasmonate effects on in vitro tuberization and tuber bulking in two potato cultivars (Solanum tuberosum L.) under different media and photoperiod condition. In Vitro Cell Dev Biol - Plant 38:203–209
Puchta H, Swoboda P, Hohn B (1995) Induction of intrachromosomal homologous recombination in whole plants. Plant J 7:203–210
Rissel D, Heym PP, Thor K, Brandt W, Wessjohann LA, Peiter E (2017) No silver bullet-canonical poly (ADP-ribose) polymerases (PARPs) are no universal factors of abiotic and biotic stress resistance of Arabidopsis thaliana. Front Plant Sci 8:1–14
Rissel D, Peiter E (2019) Poly(ADP-ribose) polymerases in plant and their human counterparts: parallels and peculiarities. Int J Mol Sci 20:1–29
Samant A, Kumar VA, Kumar A, Dhukla PS, Joshi KK (2018) In vitro microtuber production in potato cultivar kufri himalini. Adv Plants Agric Res 8:648–653
Schultz P, Jansseune K, Degenkolbe T, Meret M, Claeys H, Skirycz A, Teige M, Willmitzer L, Hannah MA (2014) Poly (ADP-ribose) polymerase controls plant growth by promoting leaf cell number. PLoS One 9:e90322
Schultz P, Neukermans J, Van Der Kelen K, Mühlenbock P, Van Breusegem F, Noctor G, Teige M, Metzlaff M, Matthew M, Hannah A (2012) Chemical PARP inhibition enhances growth of Arabidopsis and reduces anthocyanin accumulation and the activation of stress protective mechanisms. PLoS One 7:e37287
Song J, Keppler BD, Wise RR, Bent AF (2015) PARP2 is the predominant poly(ADP-ribose) polymerase in Arabidopsis DNA damage and immune responses. PLoS Genet 11:e1005200
Strain AJ (1985) Inhibitors of ADP-ribosyl transferase enhance the transformation of NIH3T3 cells following transfection with SV40 DNA. Exp Cell Res 159:531–535
Su ZZ, Zhang P, Fisher PB (1990) Enhancement of viral and DNA mediated transformation of cloned rat embryo fibroblast cells by 3-aminobenzamide. Mol Carcinog 3:309–318
Trujillo C, Rodriguez-Arango E, Jaramillo S, Hoyos R, Orduz S, Arango R (2001) One-step transformation of two Andean potato cultivars Solanum tuberosum L. subsp. Andigena. Plant Cell Rep 20:637–641
Vanderauwera S, De Block M, Van de Steene N, Van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly (ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci 104:15150–15155
Visser RGF (1991) Transformation of potato. In: Lindsey K (ed) Plant Tissue Culture Manual, vol B5. Kluwer Academic Publishers, pp 1–9
Acknowledgments
We thank Andres Narvaez for assistance in figure and manuscript preparation.
Author contribution statement
MLOC conceived and designed the research, and wrote the manuscript; DJG and VJC conducted the experimental research and helped with the preparation of tables and figures; and JNV helped with data analysis and writing and manuscript preparation.
Funding
The College of Natural and Agricultural Sciences of the University of California Riverside supported this research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no conflict of interest and comply with ethical standards.
Additional information
Editor: Charles Armstrong
Rights and permissions
About this article
Cite this article
Chetty, V.J., García, D.J., Narváez-Vásquez, J. et al. Poly (ADP-ribose) polymerase inhibitor 3-methoxybenzamide enhances in vitro plant growth, microtuberization, and transformation efficiency of blue potato (Solanum tuberosum L. subsp. andigenum). In Vitro Cell.Dev.Biol.-Plant 56, 833–841 (2020). https://doi.org/10.1007/s11627-020-10086-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-020-10086-9