Proteome study of embryogenic competence acquisition in the callus cultures of Nothapodytes nimmoniana (J. Graham) Mabberly

• Autorzy: Isah T. , Umar S.
• Języki publikacji: EN

Abstrakty

EN

Among the alternative plant sources of camptothecin (CPT), Nothapodytes nimmoniana is regarded as the most convenient source for large-scale isolation of the monoterpenoid indole anticancer alkaloid. As a result, CPT annual trade value has grossed over billion US Dollars in recent years. Somatic embryogenesis (SE) offers potential application in the rapid clonal propagation of the tree and production of the alkaloid, so as to mitigate indiscriminate harvest of its endangered natural population to meet industrial demand. However, response to the production of embryogenic callus (EC) in the in vitro cultures of N. nimmoniana is poor to scant. In the present study, two-dimensional electrophoresis (2-DE) and mass spectrometry (MaSp/MaSp) were employed in studying proteome expression changes between EC and non-embryogenic callus (NEC) of the forest tree. The results of the study showed higher metabolic and physiological processes associated with embryogenic competence acquisition in the callus cultures; high cellular oxidative stress, energy metabolism, protein synthesis, and other metabolic processes played a key role in upregulated expression of the identified proteins in EC over NEC. Putative role of the expressed proteins during embryogenic competence acquisition by N. nimmoniana callus cultures has provided some insight into the physiology of the competence acquisition through cellular roles played by oxidative stress and metabolic processes. Further studies on metabolic physiological processes associated with EC production could have application in optimizing culture conditions for mass propagation through the SE, so as to mitigate the indiscriminate harvest of endangered N. Nimmoniana natural population for CPT.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 06
• Opis fizyczny: Article 96 [16p.], fig.,ref.

Twórcy

autor

Isah T.

• Department of Botany, School of Chemical and Life Sciences, Hamdard University New Delhi, Delhi 110 062, India

autor

Umar S.

• Department of Botany, School of Chemical and Life Sciences, Hamdard University New Delhi, Delhi 110 062, India

Bibliografia

• Ali M, Isah T, Mujib A, Dipti T (2016) Climber plants: medicinal importance and conservation strategies. In: Shahzad A, Sharma S, Siddiqui SA (eds) Biotechnological strategies for the conservation of medicinal and ornamental climbers. Springer, Switzerland, pp 101–138. https://doi.org/10.1007/978-3-319-19288-8
• Andrawis A, Solomon M, Delmer DP (1993) Cotton fiber annexins: a potential role in the regulation of callose synthase. Plant J 3:763–772. https://doi.org/10.1111/j.1365-313X.1993.00763.x
• Balbuena TS, Silveira V, Junqueira M et al (2009) Changes in the 2-dimensional electrophoresis protein profile during zygotic embryogenesis in the Brazilian Pine. J Proteomics 72(3):337–352. https://doi.org/10.1016/j.jprot.2009.01.011
• Boradia VM, Raje M, Raje CI (2014) Protein moonlighting in iron metabolism: glyceraldehyde-3-phosphate dehydrogenase (GAPDH). Biochem Soc Trans 42(6):1796–1801. https://doi.org/10.1042/BST20140220
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7(72):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
• Caruso G, Cavaliere C, Guarino C et al (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis (2DE) and MALDI-TOF mass spectrometry. Anal Bioanal Chem 391:381–390. https://doi.org/10.1007/s00216-008-2008-x
• Chapman KD, Venables BJ, Blair R, Bettinger C (1999) N-Acylethanolamines in seeds: quantification of molecular species and their degradation upon imbibition. Plant Physiol 120:1157–1164. https://doi.org/10.1104/pp.120.4.1157
• Chen K, Wu HJ, Chen JF (2012) Somatic embryogenesis and mass spectrometric identification of proteins related to somatic embryogenesis in Eruca sativa. Plant Biotechnol Rep 6:113–122. https://doi.org/10.1007/s11816-011-0203-2
• Chong-Perez B, Reyes M, Rojas L et al (2012) Establishment of embryogenic cell suspension cultures and Agrobacterium-mediated transformation in banana cv. ‘Dwarf Cavendish’ (Musa AAA): effect of spermidine on transformation efficiency. Plant Cell Tiss Organ Cult 111:79–90. https://doi.org/10.1007/s11240-012-0174-1
• de Carvalho Silva R, Carmo LST, Luis ZG, Silva LP, Scherwinski-Pereira JE, Mehta A (2014) Proteomic identification of differentially expressed proteins during the acquisition of somatic embryogenesis in oil palm (Elaeis guineensis Jacq.). J Proteomics 104:112–127. https://doi.org/10.1016/j.jprot.2014.03.013
• Fulzele DP, Satdive RK (2003) Somatic embryogenesis, plant regeneration and evaluation of the camptothecin content in Nothapodytes foetida. Cell Dev Biol Plant 39(2):212–216. https://doi.org/10.1079/ivp2002368
• Fulzele DP, Satdive RK (2005) Comparison of techniques for the extraction of the anticancer drug camptothecin from Nothapodytes foetida. J Chromatogr Anal 1063(1–2):9–13. https://doi.org/10.1016/j.chroma.2004.11.020
• Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis in Arabidopsis. Planta 222(6):977–988. https://doi.org/10.1007/s00425-005-0041-y
• Giri CC, Shyamkumar B, Anjaneyulu A (2004) Progress in tissue culture, genetic transformation and applications of biotechnology to trees: an overview. Trees 18:115–135. https://doi.org/10.1007/s00468-003-0287-6
• Gomez-Garay A, Lopez JA, Camafeitab E et al (2013) Proteomic perspective of Quercus suber somatic embryogenesis. J Proteomics 93:314–325. https://doi.org/10.1016/j.jprot.2013.06.006
• Govindachari TR, Viswanathan N (1972) The alkaloids of Mappia foetida. Phytochem 11(12):3529. https://doi.org/10.1016/S0031-9422(00)89852-0
• Gupta PK, Timmis R, Pullman G et al (1991) Development of an embryogenic system for automated propagation of forest trees. In: Vasil I (ed) Scale-up and automation in plant propagation. Academic press Inc., New York, pp 75–80. https://doi.org/10.1016/b978-0-12-715008-6.50011-7
• Heringer AS, Barroso T, Macedo AF et al (2015) Label-free quantitative proteomics of embryogenic and non-embryogenic callus during sugarcane somatic embryogenesis. PLoS One 10(6):e0127803. https://doi.org/10.1371/journal.pone.0127803
• Imin N, De Jong F, Mathesius U et al (2004) Proteome reference maps of Medicago truncatula embryogenic cell cultures generated from single protoplasts. Proteomics 4:1883–1896. https://doi.org/10.1002/pmic.200300803
• Imin N, Nizamudin M, Daniher D et al (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula explant cultures grown under N⁶-benzylaminopurine and 1-naphthalene acetic acid treatments. Plant Physiol 137:1250–1260. https://doi.org/10.1104/pp.104.055277
• Isaacson T, Damasceno CM, Saravanan RS et al (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1(2):769–774. https://doi.org/10.1038/nprot.2006.102
• Isah T (2015) Adjustments to in vitro culture conditions and associated anomalies in plants. Acta Biol Crac Ser Bot 57(2):9–28. https://doi.org/10.1515/abcsb-2015-0026
• Isah T (2016a) Induction of somatic embryogenesis in woody plants. Acta Physiol Plant 38:118. https://doi.org/10.1007/s11738-016-2134-6
• Isah T (2016b) Anticancer alkaloids from trees: development into drugs. Pharmacogn Rev 10(20):90. https://doi.org/10.4103/0973-7847.194047
• Isah T (2017) Production of camptothecin in the elicited callus cultures of Nothapodytes nimmoniana (J. Graham) Mabberly. Chem Papers 71:1091–1106. https://doi.org/10.1007/s11696-016-0056-9
• Isah T (2019) Proteome study of somatic embryogenesis in Nothapodytes nimmoniana. 3 Biotech 9(4):119. https://doi.org/10.1007/s13205-019-1637-4
• Isah T, Mujib A (2012) Studies on antioxidant enzymes activity during in vitro morphogenesis of Caladium bicolor Linn. Int J Mod Cell Mol Biol 1(1):1–9
• Isah T, Mujib A (2015a) Camptothecin from Nothapodytes nimmoniana: review on biotechnology applications. Acta Physiol Plant 37:106. https://doi.org/10.1007/s11738-015-1854-3
• Isah T, Mujib A (2015b) In vitro propagation and camptothecin production in Nothapodytes nimmoniana. Plant Cell Tiss Organ Cult 121:1–10. https://doi.org/10.1007/s11240-014-0683-1
• Isah T, Mujib A (2015c) Enhanced in vitro seedling recovery in Nothapodytes nimmoniana. Br Biotechnol J 6(1):2231–2927. https://doi.org/10.9734/bbj/2015/15368
• Isah T, Umar S (2018) Influencing in vitro clonal propagation of Chonemorpha fragrans (Moon) Alston by culture media strength, plant growth regulators, carbon source and photoperiodic incubation. J For Res 5:55. https://doi.org/10.1007/s11676-018-0794-3
• Isah T, Umar S, Mujib A et al (2018) Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell Tiss Organ Cult 132:239–265. https://doi.org/10.1007/s11240-017-1332-2
• Kadrmas JL, Beckerle MC (2004) The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5:920–931. https://doi.org/10.1038/nrm1499
• Kai G, Wu C, Gen L, Zhang L, Cui L, Ni X (2015) Biosynthesis and biotechnological production of anticancer drug camptothecin. Phytochem Rev 14(3):525–539. https://doi.org/10.1007/s11101-015-9405-5
• Karami O, Aghavaisi B, Pour AM (2009) Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2:177–190. https://doi.org/10.1007/s12154-009-0028-4
• Khadke S, Kuvalekar A (2013) Direct somatic embryogenesis and plant regeneration from leaf and stem explants of Nothapodytes foetida: a critically endangered plant species. Int J Plant Anim Environ Sci 3(1):257–264
• Kurczynska EU, Gaj MD, Ujczak A, Mazur E (2007) Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh. Planta 226:619–628. https://doi.org/10.1007/s00425-007-0510-6
• Kutchan T (1995) Alkaloid biosynthesis: the basis for metabolic engineering of medicinal plants. Plant Cell 7:1059–1070. https://doi.org/10.1105/tpc.7.7.1059
• Li K, Zhu W, Zeng K et al (2010) Proteome characterization of cassava (Manihot esculenta Crantz) somatic embryos, plantlets and tuberous roots. Proteome Sci 27(8):10. https://doi.org/10.1186/1477-5956-8-10
• Lippert D, Zhuang J, Ralph S et al (2005) Proteome analysis of the early somatic embryogenesis in Picea glauca. Proteomics 5:461–473. https://doi.org/10.1002/pmic.200400986
• Lorence A, Nessler CL (2004) Camptothecin, over four decades of surprising findings. Phytochem 65(20):2735–2749. https://doi.org/10.1016/j.phytochem.2004.09.001
• Ludwig-Müller J (2011) Auxin conjugates: their role in plant development and the evolution of land plants. J Exp Bot 62(6):1757–1773. https://doi.org/10.1093/jxb/erq412
• Lulsdorf MM, Tautorus TE, Kikcio SI, Dunstan DI (1992) Growth parameters of embryogenic suspension culture of interior spruce (Picea glauca-engelmannii complex) and black spruce (Picea mariana Mill.). Plant Sci 82:227–234. https://doi.org/10.1016/0168-9452(92)90224-A
• Lutz JD, Wong JR, Rowe J et al (1985) Somatic embryogenesis for mass cloning of crop plants. In: Henke RR et al (eds) Tissue culture in forestry and agriculture: basic life sciences, vol 32. Springer, Washington, pp 105–116. https://doi.org/10.1007/978-1-4899-0378-5_8
• Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116:3051–3060. https://doi.org/10.1242/jcs.00653
• Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Ann Rev Plant Physiol Plant Mol Biol 47:127–158. https://doi.org/10.1146/annurev.arplant.47.1.127
• Marsoni M, Bracale M, Espen L et al (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27:347–356. https://doi.org/10.1007/s00299-007-0438-0
• Merkulova M, Hurtado-Lorenzo A, Hosokawa H et al (2011) Aldolase directly interacts with ARNO and modulates cell morphology and acid vesicle distribution. Am J Physiol Cell Physiol 300(6):1442–1455. https://doi.org/10.1152/ajpcell.00076.2010
• Minocha R, Minocha SC, Long S (2004) Polyamines and their biosynthetic enzymes during somatic embryo development in red spruce (Picea rubens Sarg.). Cell Dev Biol Plant 40(6):572–580. https://doi.org/10.1079/ivp2004569
• Mujib A, Ali M, Isah T, Dipti T (2014) Somatic embryo mediated mass production of Catharanthus roseus in culture vessel (bioreactor)—a comparative study. Saudi J Biol Sci 21(5):442–449. https://doi.org/10.1016/j.sjbs.2014.05.007
• Mujib A, Ali M, Dipti T, Isah T, Zafar N (2016) Embryogenesis in ornamental monocots: plant growth regulators as signaling element. In: Mujib A (ed) Somatic embryogenesis in ornamentals and its applications. Springer, New Delhi, pp 187–201. https://doi.org/10.1007/978-81-322-2683-3_12
• Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15(3):473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
• Namasivayam P (2007) Acquisition of embryogenic competence during somatic embryogenesis. Plant Cell Tiss Organ Cult 90:1–8
• Noah AM, Niemenak N, Sunderhaus S et al (2013) Comparative proteomic analysis of early somatic and zygotic embryogenesis in Theobroma cacao L. J Proteomics 78:123–133. https://doi.org/10.1016/j.jprot.2012.11.007
• Nogueira F, Goncalves E, Jereissati E et al (2007) Proteome analysis of embryogenic cell suspensions of cowpea (Vigna unguiculata). Plant Cell Rep 26:1333–1343. https://doi.org/10.1007/s00299-007-0327-6
• Normanly J, Slovin JP, Cohen JD (2004) Auxin biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action. Kluwer Academic Publishers, Dordrecht, pp 36–62
• O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021
• Padmanabha BV, Chandrashekar M, Ramesha BT et al (2006) Patterns of accumulation of camptothecin, an anti-cancer alkaloid in Nothapodytes nimmoniana Graham., in the Western Ghats, India: implications for identifying high-yielding sources of the alkaloid. Curr Sci Bangalore 90(1):95
• Pan Z, Guan R, Zhu S, Deng X (2009) Proteomic analysis of somatic embryogenesis in Valencia sweet orange. Plant Cell Rep 28:281–289
• Prakash L, Middha SK, Mohanty SK, Swamy MK (2016) Micropropagation and validation of genetic and biochemical fidelity among regenerants of Nothapodytes nimmoniana (Graham) Mabb. employing ISSR markers and HPLC. 3 Biotech 6(2):171. https://doi.org/10.1007/s13205-016-0490-y
• Ramesha BT, Amna T, Ravikanth G et al (2008) Prospecting for camptothecines from Nothapodytes nimmoniana in the Western Ghats, South India: identification of high-yielding sources of camptothecin and new families of camptothecines. J Chromatogr Sci 46(4):362–368. https://doi.org/10.1093/chromsci/46.4.362
• Ressad F, Didry D, Egile C, Pantaloni D, Carlier MF (1999) Control of actin filament length and turnover by actin depolymerizing factor (ADF/cofilin) in the presence of capping proteins and ARP2/3 complex. J Biol Chem 274:20970–20976
• Rider SD, Henderson JT, Jerome RE (2003) Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 35(1):33–43. https://doi.org/10.1046/j.1365-313X.2003.01783.x
• Savic B, Tomic S, Magnus V et al (2009) Auxin amidohydrolases from Brassica rapa cleave the alanine conjugate of indole propionic acid as a preferable substrate: a biochemical and modeling approach. Plant Cell Physiol 50(9):1587–1599. https://doi.org/10.1093/pcp/pcp101
• Strzalka W, Ziemienowicz A (2011) Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann Bot 107(7):1127–1140. https://doi.org/10.1093/aob/mcq243
• Suhas S, Ramesha BT, Ravikanth G et al (2007) Chemical profiling of Nothapodytes nimmoniana populations in the Western Ghats, India for anti-cancer compound, camptothecin. Curr Sci 92(8):1142–1147
• Sun L, Wu Y, Zou H (2013) Comparative proteomic analysis of the H99 inbred maize (Zea mays L.) line in embryogenic and non-embryogenic callus during somatic embryogenesis. Plant Cell Tiss Organ Cult 113:103–119. https://doi.org/10.1007/s11240-012-0255-1
• Tao L, Yang Y, Wang Q, You X (2012) Callose deposition is required for somatic embryogenesis in plasmolyzed Eleutherococcus senticosus zygotic embryos. Int J Mol Sci 13(11):14115–14126. https://doi.org/10.3390/ijms131114115
• Tarze A, Deniaud A, Le Bras M et al (2007) GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 26(18):2606–2620. https://doi.org/10.1038/sj.onc.1210074
• Zala D, Hinckelmann MV, Yu H et al (2013) Vesicular glycolysis provides on-board energy for the fast axonal transport. Cell 152(3):479–491. https://doi.org/10.1016/j.cell.2012.12.029
• Zhang JW, Ma HQ, Chen S et al (2009) Stress response proteins’ differential expression in embryogenic and non-embryogenic callus of Vitis vinifera L. cv. Cabernet Sauvignon—a proteomic approach. Plant Sci 177:103–113. https://doi.org/10.1016/j.plantsci.2009.04.003

Identyfikatory

DOI

10.1007/s11738-019-2896-8