Toward evaluation of the monolignol biosynthesis gene network with contemplation on the role of cinnamoyl coA reductase (CCR) gene family in camelina sativa

Document Type : Research Paper

Authors

1 Department of Agricultural Biotechnology, National Institute of Genetic Engineering and Biotechnology,Tehran, Iran.

2 Department of Biology, Faculty of Science, University of Sistan va Baluchestan, Zahedan, Iran.

3 Associate Professor, Department of Agricultural Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran.

Abstract

 
Objective
Camelina (Camelina sativa L. Crantz) is a fast-growing oil crop belonging to the Brassicaceae family that can tolerate drought, salinity, cold, and many diseases and pests. Camelina seed has precious oil and protein with a number of potential attributes or benefits in both the human food and animal feed industry. Camelina also is being deemed as promising species to produce biodiesel and jet fuel in margin lands of the globe. Monolignols, as the precursor of lignin, are the common compounds in both lignification and soluble chemicals that have important roles in both normal development of healthy plants and defense-related responses in infected plant subjects. The regulatory mechanisms underlying the biosynthesis of these multifaceted secondary metabolites are poorly understood.
 
 
Material and Methods
Our current study presents the mode of gene expression and analyzes data to investigate the role of monolignol biosynthesis genes in the normal development growth of Camelina. We considered the transcript level of those genes that were covered 12 different tissues in major developmental stages during the life cycle of the Camelina. Using the R programming environment, we could have visualized the pattern of gene expressions with transcript per million (TPM) data in the heatmap. 
 
Results
The results revealed the similarities as well as differences in gene expression patterns in both regulatory and functional gene groups among different tissues. Moreover, tissue-specific genes in different developmental stages were recognized. 
 
Conclusions
The scrutiny in the literature related on biotic stress experiments in Camelina and also other species determined considerable differences in transcript levels and gene regulation patterns for the genes especially for members of the gene group encoding cinnamoyl-CoA reductase (CCR). Association of the latter genes CsCCR4 and CsCCR2 in particular involved in monolignol biosynthesis with the resistance of Camelina to pathogens contributes to providing a preliminary view to contemplate the future research options in various Camelina breeding programs.

Keywords


 
References 
Anderson DM, MacPherson MJ, Collins SA et al. (2018) Yellow-and brown-seeded canola (Brassica napus), camelina (Camelina sativa) and Ethiopian mustard (Brassica carinata) in practical diets for rainbow trout fingerlings. J Appl Aquac 30, 187-195.
Augustin JM, Higashi Y, Feng X et al. (2015) Production of mono-and sesquiterpenes in Camelina sativa oilseed. Planta 242, 693-708.
Balanuca B, Stan R, Hanganu A et al. (2015) Design of new camelina oil-based hydrophilic monomers for novel polymeric materials. JAOCS 92, 881-891.
Bayat A, Kairenius P, Stefański T et al. (2015) Effect of camelina oil or live yeasts (Saccharomyces cerevisiae) on ruminal methane production, rumen fermentation, and milk fatty acid composition in lactating cows fed grass silage diets. J. Dairy Sci. 98, 3166-3181.
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu. Rev Plant Biol 54, 519-546.
Bosch M, Mayer C-D, Cookson A et al. (2011) Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. Annu. Rev Plant Biol 62, 3545-3561.
Brandao V, Dai X, Paula E et al. (2018) Effect of replacing calcium salts of palm oil with camelina seed at 2 dietary ether extract levels on digestion, ruminal fermentation, and nutrient flow in a dual-flow continuous culture system. J Dairy Sci 101, 5046-5059.
Bray EA (2002) Classification of genes differentially expressed during water‐deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot 89, 803-811.
Buell C, Somerville S (1995) Expression of defense-related and putative signaling genes during tolerant and susceptible interactions of Arabidopsis with Xanthomonas campestris pv. campestris. MPMI 8, 435-443.
Campos ML, Yoshida Y, Major IT et al. (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat Commun 7, 12570.
Cosio C, Ranocha P, Francoz E et al. (2017) The class III peroxidase PRX 17 is a direct target of the MADS‐box transcription factor AGAMOUS‐LIKE15 (AGL 15) and participates in lignified tissue formation. New Phytol 213, 250-263.
Derikvand MM, Sierra JB, Ruel K et al. (2008) Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227, 943-956.
Dixon RA, Barros J (2019) Lignin biosynthesis: old roads revisited and new roads explored. Open Biol 9, 190215.
Dixon RA, Chen F, Guo D et al. (2001) The biosynthesis of monolignols: a “metabolic grid”, or independent pathways to guaiacyl and syringyl units? Phytochem 57, 1069-1084.
Eynck C, SÉGUIN‐SWARTZ G, Clarke WE et al. (2012) Monolignol biosynthesis is associated with resistance to Sclerotinia sclerotiorum in Camelina sativa. Mol Plant Pathol 13, 887-899.
Ferrie A, Bethune T (2011) A microspore embryogenesis protocol for Camelina sativa, a multi-use crop. PCTOC 106, 495-501.
Gallego-Giraldo L, Escamilla-Trevino L, Jackson LA et al. (2011) Salicylic acid mediates the reduced growth of lignin down-regulated plants. PNAS 108, 20814-20819.
Halpin C (2019) Lignin engineering to improve saccharification and digestibility in grasses. Curr Opin Biotechnol 56, 223-229.
Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol. 5, 224-229.
Jiang J, Zhao X, Tian W et al. (2009) Intertribal somatic hybrids between Brassica napus and Camelina sativa with high linolenic acid content. PCTOC 99, 91-95.
Juodka R, Juška R, Juškienė V et al. (2018) The effect of feeding with hemp and Camelina cakes on the fatty acid profile of duck muscles. Arch Anim Breed, 293-303.
Kagale S, Koh C, Nixon J et al. (2014) The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Commun 5, 3706.
Kagale S, Nixon J, Khedikar Y et al. (2016) The developmental transcriptome atlas of the biofuel crop Camelina sativa. Plant J. 88, 879-894.
Keen N, Littlefield L (1979) The possible association of phytoalexins with resistance gene expression in flax to Melampsora lini. Physiol Plant Pathol 14, 265-280.
Kiefer M, Schmickl R, German DA et al. (2013) BrassiBase: introduction to a novel knowledge database on Brassicaceae evolution. Plant Cell Physiol 55, e3-e3.
König S, Feussner K, Kaever A et al. (2014) Soluble phenylpropanoids are involved in the defense response of A rabidopsis against V erticillium longisporum. New Phytol 202, 823-837.
Krohn BJ, Fripp M (2012) A life cycle assessment of biodiesel derived from the “niche filling” energy crop camelina in the USA. Appl Energy 92, 92-98.
Lacombe E, Hawkins S, Van Doorsselaere J et al. (1997) Cinnamoyl CoA reductase, the first committed enzyme of the lignin branch biosynthetic pathway: cloning, expression and phylogenetic relationships. Plant J 11, 429-441.
Lam PY, Tobimatsu Y, Takeda Y et al. (2017) Disrupting flavone synthase II alters lignin and improves biomass digestibility. Plant Physiol 174, 972-985.
Lauvergeat V, Lacomme C, Lacombe E et al. (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochem 57, 1187-1195.
Li X, Mupondwa E, Tabil L (2018) Technoeconomic analysis of biojet fuel production from camelina at commercial scale: Case of Canadian Prairies. Bioresour Technol 249, 196-205.
Lu C, Kang J (2008) Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation. Plant cell reports 27, 273-278.
Lyzenga WJ, Harrington M, Bekkaoui D et al. (2019) CRISPR/Cas9 editing of three CRUCIFERIN C homoeologues alters the seed protein profile in Camelina sativa. BMC Plant Biol 19, 292.
Menden B, Kohlhoff M, Moerschbacher BM (2007) Wheat cells accumulate a syringyl-rich lignin during the hypersensitive resistance response. Phytochem 68, 513-520.
Miedes E, Vanholme R, Boerjan W et al. (2014) The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci 5, 358.
Mierlita D, Pop IM, Lup F et al. (2018) The fatty acid composition and health lipid indices in sheep raw milk under a pasture-based dairy system. Rev Chim 69, 160-165.
Moser BR (2016) Fuel property enhancement of biodiesel fuels from common and alternative feedstocks via complementary blending. Renew Energ. 85, 819-825.
Mutuku JM, Cui S, Hori C et al. (2019) The structural integrity of lignin is crucial for resistance against Striga hermonthica parasitism in rice. Plant Physiol 179, 1796-1809.
Nelson DC, Flematti GR, Riseborough J-A et al. (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. PNAS 107, 7095-7100.
Nguyen HT, Silva JE, Podicheti R et al. (2013) Camelina seed transcriptome: a tool for meal and oil improvement and translational research. Plant Biotechnol J 11, 759-769.
Østergaard L, Lauvergeat V, Næsted H et al. (2001) Two differentially regulated Arabidopsis genes define a new branch of the DFR superfamily. Plant Sci 160, 463-472.
Parani M, Rudrabhatla S, Myers R et al. (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J. 2, 359-366.
Raes J, Rohde A, Christensen JH et al. (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133, 1051-1071.
Rogers LA, Dubos C, Cullis IF et al. (2005) Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot 56, 1651-1663.
Russo R, Reggiani R (2017) Glucosinolates and Sinapine in camelina meal. In: Food Nutr Sci pp 1063-1073.
Sarkanen KV, Ludwig CH (1971) Liguins. Occurrence, formation, structure, and reactions.
Sarry JE, Kuhn L, Ducruix C et al. (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. J Proteom 6, 2180-2198.
Schmid M, Davison TS, Henz SR et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37, 501.
Service FA (2019) oilseed world markets and trade. United States Department of Agriculture 
Sigareva M, Earle E (1997) Intertribal somatic hybrids between Camelina sativa and rapid cycling Brassica oleracea. Cruciferae Newsletter (United Kingdom).
Smil V (2016) Energy transitions: global and national perspectives. ABC-CLIO.
Vanholme R, Morreel K, Darrah C et al. (2012) Metabolic engineering of novel lignin in biomass crops. New Phytol 196, 978-1000.
Wang Y, Chantreau M, Sibout R et al. (2013) Plant cell wall lignification and monolignol metabolism. Front Plant Sci 4, 220.
Wei L, Jian H, Lu K et al. (2017) Genetic and transcriptomic analyses of lignin-and lodging-related traits in Brassica napus. Theor Appl Genet 130, 1961-1973.
Wuyts N, Lognay G, Swennen R et al. (2006) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57, 2825-2835.
Yoon J, Cho L-H, Antt HW et al. (2017) KNOX protein OSH15 induces grain shattering by repressing lignin biosynthesis genes. Plant Physiol 174, 312-325.
Zheng M, Chen J, Shi Y et al. (2017) Manipulation of lignin metabolism by plant densities and its relationship with lodging resistance in wheat. Sci Rep 7, 1-12.
Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18, 3158-3170.
Zhou J, Lee C, Zhong R et al. (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21, 248-266.