Development of rapid and genotype-independent in vitro adventitious shoot differentiation in C4 bioenergy crop Cenchrus ciliaris L.

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Keywords: Adventitious shoot, Apomictic, Shoot apical meristem, Shoot organogenesis, Ontogeny


Abstract


A highly rapid, efficient and consistent protocol for direct adventitious shoot induction, without a callus stage, was successfully established from seed-derived in vitro shoot apices of eight genotypes of Cenchrus ciliaris. Multiple shoots were induced on Murashige and Skoog (MS) containing 1–5 mg L−1 thidiazuron (TDZ). Additional cytokinins [6-benzyladenine (BA) and kinetin] were also tried for shoot induction but only TDZ was effective compared to others in promoting shoot development within 2–3 weeks of culture initiation. After two weeks of culture, 93.3 per cent of mean shoot formation was observed on MS medium (with 3.0 mg L−1 TDZ, 30 g L−1 sucrose, and 0.8% agar). The number of shootlets produced per shoot apex was significantly influenced by the use of different cytokinins and genotypes. Of all the cytokinins, the percentage shoot induction (93.3) and number of shoots induced were maximum (19.5) with TDZ at 3 mg L−1 in genotype IG-3108. Well-grown shoots were rooted (90%) on MS with 2 mg L−1 Indole-3-butyric acid (IBA). The well-rooted complete plantlets were transferred to soil in pots, where they grew normally. Histological observations helped to understand the pattern of adventitious shoot differentiation from the single shoot apex meristem. Also from histology, transverse sections confirmed that adventitious shoots had originated from the continuous vascular connection. This regeneration pathway could be another potential tool to optimize the genetic transformation of apomictic C. ciliaris.


Adventitious shoot, Apomictic, Shoot apical meristem, Shoot organogenesis, Ontogeny


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References


Abdullah AA, Grace J (1987) Regeneration of calabrian pine from juvenile needles. Plant Sci 53:147–155. https://doi.org/10.1016/0168-9452(87)90124-5


Arockiasamy S, Ignacimuthu S (2007) Regeneration of transgenic plants from two indica rice (Oryza sativa L.) cultivars using shoot apex explants. Plant Cell Rep 26(10):1745. https://doi.org/10.1007/s00299-007-0377-0


Ather A, Khan S, Rehman A, Nazir M (2009) Optimization of the protocols for callus induction, regeneration and acclimatization of sugarcane cv thatta-10. Pak J Bot 41(2):815–820


Babu GA, Vinoth A, Ravindhran R (2018) Direct shoot regeneration and genetic fidelity analysis in finger millet using ISSR markers. Plant Cell Tissue Organ Cult 132(1):157–164. https://doi.org/10.1007/s11240-017-1319-z


Barker W, Steward F (1962) Growth and development of the banana plant. II. The transition from the vegetative to the floral shoot in Musa acuminata cv. Gros Michel Ann Bot 26:413–423. https://doi.org/10.1093/oxfordjournals.aob.a083803


Berners-Lee M, Kennelly C, Watson R, Hewitt CN (2018) Current global food production is sufficient to meet human nutritional needs in 2050 provided there is radical societal adaptation. Elem Sci Anth 1:6. https://doi.org/10.1525/elementa.310


Bhat V, Dalton SJ, Kumar S, Bhat BV, Gupta MG, Morris P (2001) Particle-inflow-gun-mediated genetic transformation of buffelgrass (Cenchrus ciliaris L.): optimizing biological and physical parameters. J Appl Genet 42:405–412


Bhatia R, Gallagher JA, Gomez LD, Bosch M (2017) Genetic engineering of grass cell wall polysaccharides for biorefining. Plant Biotechnol J 15:1071–1092


Bregitzer P, Tonks D (2003) Inheritance and expression of transgenes in barley. Crop Sci 43:4–12. https://doi.org/10.2135/cropsci2003.4000


Burner DM, Grisham MP (1995) Induction and stability of phenotypic variation in sugarcane as affected by propagation procedure. Crop Sci 35:875–880. https://doi.org/10.2135/cropsci1995.0011183X003500030040x


Cassidy ES, West PC, Gerber JS, Foley JA (2013) Redefining agricultural yields: from tonnes to people nourished per hectare. Environ Res Lett 8:034015. https://doi.org/10.1088/1748-9326/8/3/034015


Cho MJ, Choi H, Okamoto D, Zhang S, Lemaux P (2003a) Expression of green fluorescent protein and its inheritance in transgenic oat plants generated from shoot meristematic cultures. Plant Cell Rep 21(5):467–474. https://doi.org/10.1007/s00299-002-0542-0


Cho MJ, Choi H, Okamoto D, Zhang S, Lemaux P (2003b) Expression of green fluorescent protein and its inheritance in transgenic oat plants generated from shoot meristematic cultures. Plant Cell Rep 21:467–474. https://doi.org/10.1007/s00299-002-0542-0


Choi HW, Lemaux PG, Cho MJ (2000) Increased chromosomal variation in transgenic versus non-transgenic barley (Hordeum vulgare) plant. Crop Sci 40:524–533. https://doi.org/10.2135/cropsci2000.402524x


Colomba EL, Grunberg K, Griffa S, Ribotta A, Mroginski L, Biderbost E (2006) The effect of genotype and culture medium on somatic embryogenesis and plant regeneration from mature embryos of fourteen apomictic cultivars of buffelgrass (Cenchrus ciliaris L.). Grass Forage Sci 6:2–8. https://doi.org/10.1111/j.1365-2494.2006.00499.x


Costa RM, Pattathil S, Avci U, Winters A, Hahn MG, Bosch M (2019) Desirable plant cell wall traits for higher-quality Miscanthus lignocellulosic biomass. Biotechnol Biofuels 12:1–8


Davis SC, Parton WJ, Grosso SJ, Keough C, Marx E, Adler PR, DeLucia EH (2012) Impact of second-generation biofuel agriculture on greenhouse-gas emissions in the corn-growing regions of the US. Front Ecol Environ 10:69–74. https://doi.org/10.1890/110003


Detrez C, Tetu T, Sangwan RS, Sangwan-Norreel BS (1988) Direct organogenesis from petiole and thin cell layer explants in sugar beet cultured in vitro. J Exp Bot 39:917–926. https://doi.org/10.1093/jxb/39.7.917


Dey T, Saha S, Ghosh PD (2015) Somaclonal variation among somatic embryo derived plants-evaluation of agronomically important somaclones and detection of genetic changes by RAPD in Cymbopogon winterianus. South Afr J Bot 96(112–2):1. https://doi.org/10.1016/j.sajb.2014.10.010


Dwivedi A, Kumar K, Verma PK (2019) Constructing synthetic pathways in plants: Strategies and tools. In: Singh SP, Pandey A, Du G, Kumar S (eds) Current Developments in Biotechnology and Bioengineering, Synthetic Biology. Elsevier, Cell Engineering and Bioprocessing Technologies


Evans SG, Ramage BS, Di Rocco TL, Potts MD (2015) Greenhouse gas mitigation on marginal land: A quantitative review of the relative benefits of forest recovery versus biofuel production. Environ Sci Technol 49:2503–2511. https://doi.org/10.1021/es502374f


FAOSTAT, (2021) Food Balances (FAO); https://www.fao.org/faostat/en/#data/FBSH


Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P (2008) Land clearing and the biofuel carbon debt. Science 319:1235–1238. https://doi.org/10.1126/science.1152747


Ganeshan S, Båga M, Harvey BL, Rossnagel BG, Scoles GJ, Chibbar RN (2003) Production of multiple shoots from thidiazuron-treated mature embryos and leaf-base/apical meristems of barley (Hordeum vulgare L.). Plant Cell Tissue Organ Cult 73:57–64. https://doi.org/10.1023/A:1022631807797


Gonbad RA, Sinniah UR, Aziz MA, Mohamad R (2014) Influence of cytokinins in combination with GA3 on shoot multiplication and elongation of tea clone Iran 100 (Camellia sinensis (L.) O. Kuntze). Sci World J 2014:1–9. https://doi.org/10.1155/2014/943054


Gupta SD, Conger BV (1998) In vitro differentiation of multiple shoot clumps from intact seedlings of switchgrass. In Vitro Cell Dev Biol Plant 34:196–202


Harris PJ, Smith BG (2006) Plant cell walls and cell-wall polysaccharides: structures, properties and uses in food products. Int J Food Sci Technol 41:129–143. https://doi.org/10.1111/j.1365-2621.2006.01470.x


Hoagland M, Arnon DI, (1950) The water culture method to grow plants without soil. Calif Agric Expt Station Cir 347. Berkeley California.


Hojsgaard D (2020) Apomixis technology: Separating the wheat from the chaff. Genes 11(4):411. https://doi.org/10.3390/genes11040411


Hojsgaard D, Hörandl E (2019) The rise of apomixis in natural plant populations. Front Plant Sci 10:358. https://doi.org/10.3389/fpls.2019.00358


Jha P, Shashi RA, Agnihotri PK, Kulkarni VM, Bhat V (2011) Efficient agrobacterium-mediated transformation of Pennisetum glaucum (L.) R. Br. using shoot apices as explant source. Plant Cell Tissue Organ Cult 107(3):501–512. https://doi.org/10.1007/s11240-011-0001-0


Jha P, Yadav CB, Anjaiah V, Bhat V, (2009) In vitro plant regeneration through somatic embryogenesis and direct shoot organogenesis in Pennisetum glaucum (L.) R.Br. In Vitro Cell Dev Biol Plant 45 (2) 145–154. https://doi.org/10.1007/s11627-009-9198-6


Jha P, Shashi, Kulkarni V, Bhat V (2016) Thidiazuron-induced multiple shoot regeneration and in vitro flowering in Pennisetum glaucum (L.) R. Br. Phytomorph: Int J Plant Morph 66 (1–2)45–50.


Johnsen DA (1940) Plant micro-techniques. McGraw-Hill, New York


Kato A, Birchler JA (2006) Induction of tetraploid derivatives of maize inbred lines by nitrous oxide gas treatment. J Hered 97(1):39–44. https://doi.org/10.1093/jhered/esj007


Kazuhiro N, Hattori K (1995) Histological observation of multiple shoot formation site in rice seed culture. Breed Sci 45(1):51–56. https://doi.org/10.1270/jsbbs1951.45.51


Khan FA, Khan A, Azhar FM, Rauf S (2009) Genetic diversity of Saccharum officinarum accessions in Pakistan as revealed by random amplified polymorphic DNA. Genet Mol Res 8(4):1376–1382


Kim S, Da K, Mei C (2012) An efficient system for high-quality large-scale micropropagation of Miscanthus× giganteus plants. In Vitro Cell Dev Biol Plant 48:613–619


Kline KL, Msangi S, Dale VH, Woods J, Souza GM, Osseweijer P, Clancy JS, Hilbert JA, Johnson FX, McDonnell PC, Mugera HK (2017) Reconciling food security and bioenergy priorities for action. GCB Bioenerg 9(3):557–576. https://doi.org/10.1111/gcbb.12366


Kumar S, Bhat V (2012) High-frequency direct plant regeneration via multiple shoot induction in the apomictic forage grass Cenchrus ciliaris L. In Vitro Cell Dev Biol Plant 48:241–248. https://doi.org/10.1007/s11627-012-9428-1


Kumar S, Sahu N, Singh A (2015) High-frequency in vitro plant regeneration via callus induction in a rare sexual plant of Cenchrus ciliaris L. In Vitro Cell Dev Biol Plant 51:28–34. https://doi.org/10.1007/s11627-015-9664-2


Kumar S, Agarwal K, Kothari SL, (2001) In vitro induction and enlargement of apical domes and formation of multiple shoots in finger millet, Eleusine coracana (L.) Gaertn and crowfoot grass, Eleusine indica (L.) Gaertn. Curr Sci 81: 1482–1485. https://www.jstor.org/stable/24106578


Laishram SD, Goyal S, Shashi KVM, Kumar S, Bhat V (2020) Comparative analysis of particle bombardment vs. Agrobacterium-mediated genetic transformation methods of Cenchrus ciliaris. Nucleus 63:303–312. https://doi.org/10.1007/s13237-020-00332-1


Mauser W, Klepper G, Zabel F, Delzeit R, Hank T, Putzenlechner B, Calzadilla A (2015) Global biomass production potentials exceed expected future demand without the need for cropland expansion. Nat Commun 6:8946. https://doi.org/10.1038/ncomms9946


McClean P, Grafton KF (1989) Regeneration of dry bean (Phaseolus vulgaris L.) via organogenesis. Plant Sci 60:117–122. https://doi.org/10.1016/0168-9452(89)90051-4


Mitchell RB, Schmer MR, Anderson WF, Jin V, Balkcom KS, Kiniry J, Coffin A, White P (2016) Dedicated energy crops and crop residues for bioenergy feedstocks in the central and eastern USA. Bioenergy Res 9:384–398. https://doi.org/10.1007/s12155-016-9734-2


Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497


Okole BN, Schultz FA (1996) Micro-sections of banana and plantains (Musa spp.) morphogenesis and regeneration of callus and shoot buds. Plant Sci 116:185–195. https://doi.org/10.1016/0168-9452(96)04381-6


Omidbaigi R, Yavari S, Hassani ME, Yavari S (2010) Induction of autotetraploidy in dragonhead (Dracocephalum moldavica L.) by colchicine treatment. J Fruit Ornam Plant Res 18(1):23–35


Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annu Rev Genet 41:509–537. https://doi.org/10.1146/annurev.genet.40.110405.090511


Ozias-Akins P, Akiyama Y, Hanna WW (2003) Molecular characterization of the genomic region linked with apomixis in Pennisetum/ Cenchrus. Funct Integr Genomics 3(3):94–104. https://doi.org/10.1007/s10142-003-0084-8


Perlack RD, Wright LL, Turhollow AF, Graham RL, Stokes BJ, Erbach DC (2005) Biomass as a feedstock for a bioenergy and bioproducts industry: The technical feasibility of a billion-ton annual supply. Environmental Science Division, Oak Ridge National Laboratory, Tennessee.


Piqueras A, Alburquerque N, Folta KM (2010) Explants used for the generation of transgenic plants. In: Kole C, Michler CH, Abbott AG, Hall TC (eds) Transgenic crop plants. Springer, Berlin Heidelberg


Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489. https://doi.org/10.1126/science.1114736


Rao AS, Singh KC, Wight JR (1996) Productivity of Cenchrus ciliaris in relation to rainfall and fertilization. J Range Manage 49:143–146


Rashid VA (2002) Induction of multiple shoots by thidiazuron from caryopsis cultures of minor millet (Paspalum scrobiculatum L.) and its effect on the regeneration of embryogenic callus cultures. Plant Cell Rep 21:9–13. https://doi.org/10.1007/s00299-002-0466-8


Ray DK, Sloat LL, Garcia AS, Davis KF, Ali T, Xie W (2022) Crop harvests for direct food use insufficient to meet the UN’s food security goal. Nat Food 3:367–374. https://doi.org/10.1038/s43016-022-00504-z


Robertson GP, Hamilton SK, Barham BL, Dale BE, Izaurralde RC, Jackson RD, Landis DA, Swinton SM, Thelen KD, Tiedje JM (2017) Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes. Science 356:1349–1357. https://doi.org/10.1126/science.aal2324


Roche D, Cong P, Chen Z, Hanna WW, Gustine DL, Sherwood RT, Ozias-Akins P (1999) An apospory-specific genomic region is conserved between Buffelgrass (Cenchrus ciliaris L.) and Pennisetum squamulatum Fresen. Plant J 19(2):203–208. https://doi.org/10.1046/j.1365-313X.1999.00514.x


Ross AH, Manners JM, Birch RG (1995) Embryogenic callus production, plant regeneration and transient gene expression following particle bombardment in the pasture grass, Cenchrus ciliaris (Gramineae). Aust J Bot 43(2):193–199. https://doi.org/10.1071/BT9950193


Sanford GR, Oates LG, Roley SS, Duncan DS, Jackson RD, Robertson GP, Thelen KD (2017) Biomass production a stronger driver of cellulosic ethanol yield than biomass quality. Agronomy J 109(5):1911–1922. https://doi.org/10.2134/agronj2016.08.0454


Schulze J (2007) Improvement in cereal tissue culture by thidiazuron: a review. Fruit Veg Cereal Sci Biotech 1(2):64–79


Searchinger TD, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, Tokgoz S, Hayes D, Yu TH (2008) Use of U.S. croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319:1238–1240. https://doi.org/10.1126/science.1151861


Service RF (2007) Biofuel researchers prepare to reap a new harvest. Science 315:1488–1491. https://doi.org/10.1126/science.315.5818.1488


Sharma VK, Hänsch R, Mendel RR, Schulze J (2004) A highly efficient plant regeneration system through multiple shoot differentiation from commercial cultivars of barley (Hordeum vulgare L.) using meristematic shoot segments excised from germinated mature embryos. Plant Cell Rep 23:9–16. https://doi.org/10.1007/s00299-004-0800-4


Sharma R, Geeta R, Bhat V (2014) Asynchronous male/female gametophyte development in facultative apomictic plants of Cenchrus ciliaris (Poaceae). South Afr J Bot 91:19–31


Shashi BV (2021) Enhanced somatic embryogenesis and plantlet regeneration in Cenchrus ciliaris L. In Vitro Cell Dev Biol Plant 57:499–509. https://doi.org/10.1007/s11627-020-10148-y


Singariya P, Kumar P, Mourya KK (2013) Absence of antibiotic activities of Cenchrus setigerus and Cenchrus ciliaris seed extracts in different polar solvents. J Pharm Negative Results 4:71–75. https://doi.org/10.4103/0976-9234.116756


Spiller GE (Ed) (2001) CRC Handbook of Dietary Fiber in Human Nutrition, CRC Press


Sugla T, Purkayastha J, Singh SK, Solleti SK, Sahoo L (2007) Micropropagation of Pongamia pinnata through enhanced axillary branching. In Vitro Cell Dev Biol Plant 43:409–414. https://doi.org/10.1007/s11627-007-9086-x


Uden DR, Mitchell RB, Allen CR, Guan Q, McCoy T (2013) The feasibility of producing adequate feedstock for year-round cellulosic ethanol production in an intensive agricultural fuel shed. Bioenergy Res 6:930–938. https://doi.org/10.1007/s12155-013-9311-x


United Nations, Department of Economic, Social Affairs, Population Division (2019). World Population Prospects 2019. Demographic Profiles, Vol II. United Nations Press, New York, NY, USA


Vikrant R (2002) Induction of multiple shoots by thidiazuron from caryopsis cultures of minor millet (Paspalum scrobiculatum L.) and its effect on the regeneration of embryogenic callus cultures. Plant Cell Rep 21:9–13. https://doi.org/10.1007/s00299-002-0466-8


Yadav CB, Jha P, Mahalakshmi C, Anjaiah V, Bhat V (2009) Somatic embryogenesis and regeneration of Cenchrus ciliaris genotypes from immature inflorescence explants. Biol Plant 53:603–609


Yadav CB, Anuj KS, Gupta MG, Bhat V (2012) Genetic linkage maps of the chromosomal regions associated with apomictic and sexual modes of reproduction in Cenchrus ciliaris. Mol Breed 30:239–250


Yookongkaew N, Srivatanakul M, Narangajavana J (2007) Development of genotype-independent regeneration system for transformation of rice (Oryza sativa ssp. indica). J Plant Res 120:237–245. https://doi.org/10.1007/s10265-006-0046-z


Young BA, Sherwood RT, Bashaw EC (1979) Cleared-pistil and thick-sectioning techniques for detecting aposporous apomixis in grasses. Can J Bot 57(15):1668–1672. https://doi.org/10.1139/b79-204


Zaffari GR, Kerbauy GB, Kraus JE, Romano EC (2000) Hormonal and histological studies related to in vitro banana bud formation. Plant Cell Tissue Organ Cult 63(3):187–192. https://doi.org/10.1023/A:1010611318932


Zhang S, Warkentin D, Sun B, Zhong H, Sticklen M (1996) Variation in the inheritance of expression among sub clones for unselected (uidA) and selected (bar) transgenes in maize (Zea mays L.). Theor Appl Genet 92:752–761


Zhang K, Wang J, Hu X, Yang A, Zhang J (2010) Agrobacterium-mediated transformation of shoot apices of kentucky bluegrass (Poa pratensis L.) and production of transgenic plants carrying a betA gene. Plant Cell Tissue Organ Cult 102(2):135–43. https://doi.org/10.1007/s11240-010-9713-9


Zhong H, Srinivasan C, Sticklen MB (1992) In vitro morphogenesis of corn (Zea mays L.) in vitro II. Trans differentiation of shoots, tassels, and ear primordia from corn shoots. Planta. https://doi.org/10.1007/BF00199967


Zhong H, Wang W, Sticklen M (1998) In vitro morphogenesis of Sorghum bicolor (L.) Moench: efficient plant regeneration from shoot apices. J Plant Physiol 153(5):719–26. https://doi.org/10.1016/S0176-1617(98)80226-5

 


Acknowledgements


This research was supported by the R & D grant from, the University of Delhi. This paper is presented by Shashi in partial fulfilment of requisites for a thesis of Doctor of Philosophy in Botany at the University of Delhi, India.


Author Information


Shashi
Plant Developmental Biology, Department of Botany, University of Delhi, Delhi, India

Bhat Vishnu
Plant Developmental Biology, Department of Botany, University of Delhi, Delhi, India
bhatv64@rediffmail.com