Abstract
Soil salinity can adversely affect crop quality and production. Napier grass hybrids with high cellulose and low lignin contents could be the most viable candidates for cost-effective bioethanol production. In this study, eight Napier grass hybrids with high ratios of cellulose to lignin contents were used as plant material to screen for salt tolerance. Among these, four hybrids were able to maintain chlorophyll content and leaf greenness. The crude fiber, cellulose and hemicellulose contents in the Napier Phetchaboon (NP) and Napier Yak Lampang (NL) hybrids increased under salt stress while lignin content did not change. Net photosynthetic rate and the amounts of total chlorophylls and total carotenoids of the NP hybrid were not affected by salt stress. Total fresh weight of the NL hybrid was reduced after 7 days of salt exposure while in the sensitive hybrid, this occurred after 1 day of exposure. Cellulose and lignin synthesis under salt stress is not directly correlated to cellulose (CesA2, CesA3 and CesA4) and lignin (PAL and CAD) associated genes. Of the hybrids tested under conditions of salt exposure, the NP and NL hybrids were the most salt-tolerant and most suitable for bioethanol production.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
AL-Shoaibi AA (2008) Photosynthetic response of elephant grass (Pennisetum purpureum) to NaCl salinity. J Biol Sci 8:610–615. https://doi.org/10.3923/jbs.2008.610.615
An P, Li X, Zheng Y, Matsuura A, Abe J, Eneji A, Tanimoto E, Inanaga S (2014) Effects of NaCl on root growth and cell wall composition of two soya bean cultivars with contrasting salt tolerance. J Agron Crop Sci 200:212–218. https://doi.org/10.1111/jac.12060
Basso V, Machado JC, da Silva Lédo FJ, da Costa Carneiro J, Fontana RC, Dillon AJP, Camassola M (2014) Different elephant grass (Pennisetum purpureum) accessions as substrates for enzyme production for the hydrolysis of lignocellulosic materials. Biomass Bioenerg 71:155–161. https://doi.org/10.1016/J.BIOMBIOE.2014.10.011
Cha-um S, Supaibulwatana K, Kirdmanee C (2006) Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica cv. KDML105) to salt stress by application of exogenous glycinebetaine and choline. J Agron Crop Sci 192:25–36. https://doi.org/10.1111/j.1439-037X.2006.00186.x
Cheng H, Li L, Xu F et al (2013) Expression patterns of a cinnamyl alcohol dehydrogenase gene involved in lignin biosynthesis and environmental stress in Ginkgo biloba. Mol Biol Rep 40:707–721. https://doi.org/10.1007/s11033-012-2111-0
Choi B, Chung JY, Bae H-J, Bae I, Park S, Bae H (2015) Functional characterization of cinnamyl alcohol dehydrogenase during developmental stages and under various stress conditions in kenaf (Hibiscus cannabinus L.). BioResources 11:105–125. https://doi.org/10.15376/biores.11.1.105-125
Colmenero-flores JM, Rosales MA (2014) Interaction between salt and heat stress: when two wrongs make a right. Plant, Cell Environ 37:1042–1045. https://doi.org/10.1111/pce.12229
Dasgupta S, Hossain MM, Huq M, Wheeler D (2015) Climate change and soil salinity: the case of coastal Bangladesh. Ambio 44:815–826. https://doi.org/10.1007/s13280-015-0681-5
Daud Z, Mohd Hatta MZ, Mohd Kassim AS, Aripin AM, Awang H (2014) Analysis of Napier grass (Pennisetum purpureum) as a potential alternative fibre in paper industry. Mater Res Innov 18:S6-18–S6-20. https://doi.org/10.1179/1432891714Z.000000000925
Eliana C, Jorge R, Juan P, Luis R (2014) Effects of the pretreatment method on enzymatic hydrolysis and ethanol fermentability of the cellulosic fraction from elephant grass. Fuel 118:41–47. https://doi.org/10.1016/j.fuel.2013.10.055
Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Froehlich A, Persson S (2015) A mechanism for sustained cellulose synthesis during salt stress. Cell 162:1353–1364. https://doi.org/10.1016/j.cell.2015.08.028
Frei M (2013) Lignin: characterization of a multifaceted crop component. Sci World J 2013:1–25. https://doi.org/10.1155/2013/436517
Gao J, Gu M, Niu G, Chen Y (2012) Effects of salinity on three Pennisetum cultivars. J Food Agric Environ 10:1005–1007. https://doi.org/10.1234/4.2012.3573
Gimeno J, Eattock N, Van Deynze A, Blumwald E (2014) Selection and validation of reference genes for gene expression analysis in switchgrass (Panicum virgatum) using quantitative real-time RT-PCR. PLoS One 9:1–12. https://doi.org/10.1371/journal.pone.0091474
Guerriero G, Legay S, Hausman JF (2014) Alfalfa cellulose synthase gene expression under abiotic stress: a Hitchhiker’s guide to RT-qPCR normalization. PLoS One 9:1–13. https://doi.org/10.1371/journal.pone.0103808
Hu G, Liu Y, Zhang X, Yao F, Huang Y, Ervin EH, Zhao B (2015) Physiological evaluation of alkali-salt tolerance of thirty switchgrass (Panicum virgatum) lines. PLoS One 10:1–17. https://doi.org/10.1371/journal.pone.0125305
Jeong MJ, Choi BS, Bae DW et al (2012) Differential expression of kenaf phenylalanine ammonia-lyase (PAL) ortholog during developmental stages and in response to abiotic stresses. Plant Omics 5:392–399
Kandel R, Singh HP, Singh BP, Harris-Shultz KR, Anderson WF (2016) Assessment of genetic diversity in Napier grass (Pennisetum purpureum Schum.) using microsatellite, single-nucleotide polymorphism and insertion-deletion markers from pearl millet (Pennisetum glaucum [L.] R. Br.). Plant Mol Biol Rep 34:265–272. https://doi.org/10.1007/s11105-015-0918-2
Ko CH, Yu FC, Chang FC, Yang BY, Chen WH, Hwang WS, Tu TC (2017) Bioethanol production from recovered Napier grass with heavy metals. J Environ Manage 203:1005–1010. https://doi.org/10.1016/j.jenvman.2017.04.049
Kretschemer EA, Pitman WD (2001) Germplasm resources of tropical forage grasses. In: Sotomayor-Rios A, Pitman WD (eds) Tropical forage plant: development and use. CRC Press, Florida, pp 27–40
Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166. https://doi.org/10.3390/plants4010112
Li Y, Zhang Y, Zheng H, Du J, Zhang H, Wu J, Huang H (2015) Preliminary evaluation of five elephant grass cultivars harvested at different time for sugar production. Chinese J Chem Eng 23:1188–1193. https://doi.org/10.1016/j.cjche.2015.04.016
Little A, Schwerdt JG, Shirley NJ, Khor SF, Neumann K, O’Donovan LA, Lahnstein J, Collins HM, Henderson M, Fincher GB, Burton RA (2018) Revised phylogeny of the cellulose synthase gene superfamily: insights into cell wall evolution. Plant Physiol 177:1124–1141. https://doi.org/10.1104/pp.17.01718
Liu JL, Wu N (2014) Biomass production of switchgrass in saline-alkali land. Adv Mat Res 1008–1009:93–96. https://doi.org/10.4028/www.scientific.net/AMR.1008-1009.93
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335. https://doi.org/10.3390/ijms19020335
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta c(t)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Loedkunchotipat K, Desclaux SS, Maksup S (2015) Expression analysis of cellulose synthase and phenylalanine ammonia-lyase genes in Napier grass hybrids (Pennisetum hybrid). Thai J Genet 8:167–174. https://doi.org/10.14456/tjg.2015.18
Maksup S, Supaibulwatana K, Selvaraj G (2013) High-quality reference genes for quantifying the transcriptional responses of Oryza sativa L. (ssp. indica and japonica) to abiotic stress conditions. Chin Sci Bull 58:1919–1930. https://doi.org/10.1007/s11434-013-5726-1
Mapato C, Wanapat M (2018) Comparison of silage and hay of dwarf Napier grass (Pennisetum purpureum) fed to Thai native beef bulls. Trop Anim Health Prod 50:1–5. https://doi.org/10.1007/s11250-018-1582-y
McFarlane HE, Doring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94. https://doi.org/10.1146/annurev-arplant-050213-040240
Mourasobczak J, Souza U, Mazzafera P (2011) Drought stress and changes in the lignin content and composition in Eucalyptus. BMC Proc 5(Suppl 7):P103. https://doi.org/10.1186/1753-6561-5-S7-P103
Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev 82:371–406. https://doi.org/10.1007/s12229-016-9173-y
Muthamilarasan M, Khan Y, Jaishankar J, Shweta S, Lata C, Prasad M (2015) Integrative analysis and expression profiling of secondary cell wall genes in C4 biofuel model Setaria italica reveals targets for lignocellulose bioengineering. Front Plant Sci 6:1–25. https://doi.org/10.3389/fpls.2015.00965
Negawo A, Teshome A, Kumar A, Hanson J, Jones C (2017) Opportunities for Napier grass (Pennisetum purpureum) improvement using molecular genetics. Agronomy 7:1–21. https://doi.org/10.3390/agronomy7020028
Neves GYS, Marchiosi R, Ferrarese MLL, Siqueira-Soares RC, Ferrarese-Filho O (2010) Root growth inhibition and lignification induced by salt stress in soybean. J Agron Crop Sci 196:467–473. https://doi.org/10.1111/j.1439-037X.2010.00432.x
Obembe OO, Jacobsen E, Vincken JP, Visser RGF (2009) Differential expression of cellulose synthase (CesA) gene transcripts in potato as revealed by QRT-PCR. Plant Physiol Bioch 47:1116–1118. https://doi.org/10.1016/j.plaphy.2009.07.006
Richards LA (1954) Diagnosis and improvement of saline and alkali soils. USDA Agricultural hand book 60. United States Department of Agriculture, Washington DC, USA
Rusdy M (2016) Elephant grass as forage for ruminant animals. Livestock research for rural development, vol 28, pp 1–5. http://www.lrrd.org/lrrd28/4/rusd28049.html. Accessed 18 Nov 2018
Samuga A, Joshi CP (2004) Differential expression patterns of two new primary cell wall-related cellulose synthase cDNAs, PtrCesA6 and PtrCesA7 from aspen trees. Gene 334:73–82. https://doi.org/10.1016/j.gene.2004.02.057
Shen H, Mazarei M, Hisano H, Escamilla-Trevino L, Fu C, Pu Y, Dixon RA (2013) A genomics approach to deciphering lignin biosynthesis in switchgrass. Plant Cell 25:4342–4361. https://doi.org/10.1105/tpc.113.118828
Singh BP, Singh HP, Obeng E (2013) Elephantgrass. In: Singh BP (ed) Biofuel crops: production, physiology and genetics. CABI, Wallingford, pp 271–291
Sneha S, Rishi A, Chandra S (2014) Effect of short term salt stress on chlorophyll content, protein and activities of catalase and ascorbate peroxidase enzymes in pearl millet. Amer J Plant Physiol 9:32–37. https://doi.org/10.3923/ajpp.2014.32.37
Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78. https://doi.org/10.1146/annurev.cellbio.22.022206.160206
Turano B, Tiwari UP, Jha R (2016) Growth and nutritional evaluation of Napier grass hybrids as forage for ruminants. Trop Grassl.-Forrajes Trop 4:168–178. https://doi.org/10.17138/tgft(4)168-178
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905. https://doi.org/10.1104/pp.110.155119
Wang T, McFarlane HE, Persson S (2016) The impact of abiotic factors on cellulose synthesis. J Exp Bot 67:543–552. https://doi.org/10.1093/jxb/erv488
Yasuda M, Ishii Y, Ohta K (2014) Napier grass (Pennisetum purpureum Schumach) as raw material for bioethanol production: pretreatment, saccharification, and fermentation. Biotechnol Bioprocess Eng 19:943–950. https://doi.org/10.1007/s12257-014-0465-y
Yu Q, Zhuang X, Wang W et al (2016) Hemicellulose and lignin removal to improve the enzymatic digestibility and ethanol production. Biomass Bioenerg 94:105–109. https://doi.org/10.1016/j.biombioe.2016.08.005
Acknowledgements
The authors kindly acknowledge the Faculty of Science, Silpakorn University for a research grant (Grant number SRF-JRG-2560-07), and we are very much indebted to the Nakorn Ratchasima Animal Nutrition Research and Development Center, BAND, DLD, Thailand for assistance with the analysis of lignocellulosic materials. We also appreciate Prof. Dr. Frederick W.H. Beamish (Faculty of Science, Burapha University) for English proofreading.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by P. Wojtaszek.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Maksup, S., Sengsai, S., Laosuntisuk, K. et al. Physiological responses and the expression of cellulose and lignin associated genes in Napier grass hybrids exposed to salt stress. Acta Physiol Plant 42, 109 (2020). https://doi.org/10.1007/s11738-020-03092-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-020-03092-2