Skip to main content

Natural Variation in Lignin and Pectin Biosynthesis-Related Genes in Switchgrass (Panicum virgatum L.) and Association of SNP Variants with Dry Matter Traits

Abstract

Switchgrass (Panicum virgatum), a C4 perennial grass native to North America and developed as a sustainable biofuel feedstock, occurs in two ecotypes, lowland and upland, which vary in their architecture as well as their range of adaptation. In this study, we assessed single nucleotide polymorphism (SNP) variation in 372 switchgrass genotypes for nine genes involved in lignin and pectin biosynthesis. STRUCTURE results at K = 3 differentiated the genotypes into three genetic subpopulations that corresponded largely to the previously characterized upland C1 and lowland C2 and C3 subpopulations. Out of the 146 SNPs identified, 19 SNPs were non-synonymous, including two non-conservative and common SNPs in cinnamyl alcohol dehydrogenase (CAD, Chr01N) and p-coumarate3-hydroxylase (C3H, Chr09N), two genes in the lignin biosynthesis pathway. Allele status at seven of the 19 non-synonymous SNPs, including the non-conservative SNP in C3H, was significantly associated with four dry matter traits within subpopulations. Dry matter traits appeared to be mostly dominant and three of them (acid detergent fiber, non-fiber carbohydrate, water-soluble carbohydrates) were the most frequently differentiated traits. In addition, a heterosis effect was detected at the non-conservative SNP in phenylalanine ammonia-lyase (PAL) for neutral detergent fiber. Association analysis revealed the CAD gene on Chr01N, its homoeolog on Chr01K and cinnamate 4-hydroxylase (C4H, Chr03K) as potential candidates associated with dry matter traits. Further analyses are needed to determine whether these candidate genes play a role in switchgrass lignin content and could be exploited to reduce recalcitrance in this bioenergy crop.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    McLaughlin SB, Kszos LA (2005) Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States. Biomass Bioenergy 28(6):515–535

    Google Scholar 

  2. 2.

    Vogel KP, Jung HJG (2001) Genetic modification of herbaceous plants for feed and fuel. Crit Rev Plant Sci 20(1):15–49

    Google Scholar 

  3. 3.

    Hultquist SJ, Vogel KP, Lee DJ, Arumuganathan K, Kaeppler S (1996) Chloroplast DNA and nuclear DNA content variations among cultivars of switchgrass, Panicum virgatum L. Crop Sci 36(4):1049–1052

    Google Scholar 

  4. 4.

    Lewandowski I, Scurlock JMO, Lindvall E, Christou M (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25(4):335–361

    Google Scholar 

  5. 5.

    Casler MD (2010) Changes in mean and genetic variance during two cycles of within-family selection in switchgrass. Bioenergy Research 3(1):47–54

    Google Scholar 

  6. 6.

    Casler MD, Stendal CA, Kapich L, Vogel KP (2007) Genetic diversity, plant adaptation regions, and gene pools for switchgrass. Crop Sci 47(6):2261–2273

    CAS  Google Scholar 

  7. 7.

    Cortese LM, Honig J, Miller C, Bonos SA (2010) Genetic diversity of twelve switchgrass populations using molecular and morphological markers. Bioenergy Research 3(3):262–271

    Google Scholar 

  8. 8.

    Bahri BA, Daverdin G, Xu X, Cheng JF, Barry KW, Brummer EC, Devos KM (2018) Natural variation in genes potentially involved in plant architecture and adaptation in switchgrass (Panicum virgatum L.). BMC Evol Biol 18(1):91–111

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    Evans JSMD, Sanciangco MD, Lau KH, Crisovan E, Barry K, Daum C, Hundley H, Jenkins J, Kennedy M, Kunde-Ramamoorthy G, Vaillancourt B, Acharya A, Schmutz J, Saha M, Kaeppler SM, Brummer EC, Casler MD, Buell CR (2017) Extensive genetic diversity is present within north American switchgrass germplasm. The Plant Genome 11:170055. https://doi.org/10.3835/plantgenome2017.06.0055

    CAS  Article  Google Scholar 

  10. 10.

    Missaoui AM, Paterson AH, Bouton JH (2006) Molecular markers for the classification of switchgrass (Panicum virgatum L.) germplasm and to assess genetic diversity in three synthetic switchgrass populations. Genet Resour Crop Evol 53(6):1291–1302

    CAS  Google Scholar 

  11. 11.

    Narasimhamoorthy B, Saha MC, Swaller T, Bouton JH (2008) Genetic diversity in switchgrass collections assessed by EST-SSR markers. Bioenergy Research 1(2):136–146

    Google Scholar 

  12. 12.

    Young HA, Lanzatella CL, Sarath G, Tobias CM (2011) Chloroplast genome variation in uplant and lowland switchgrass. PLoS One 6(8):e23980. https://doi.org/10.1371/journal.pone.0023980

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Zalapa JE, Price DL, Kaeppler SM, Tobias CM, Okada M, Casler MD (2011) Hierarchical classification of switchgrass genotypes using SSR and chloroplast sequences: ecotypes, ploidies, gene pools, and cultivars. Theor Appl Genet 122(4):805–817

    CAS  PubMed  Google Scholar 

  14. 14.

    Zhang Y, Zalapa JE, Jakubowski AR, Price DL, Acharya A, Wei Y, Brummer EC, Kaeppler SM, Casler MD (2011) Post-glacial evolution of Panicum virgatum: centers of diversity and gene pools revealed by SSR markers and cpDNA sequences. Genetica 139(7):933–948

    PubMed  Google Scholar 

  15. 15.

    Ali S, Serba DD, Jenkins J, Kwon S, Schmutz J, Saha MC (2019) High-density linkage map reveals QTL underlying growth traits in AP13xVS16 biparental population of switchgrass. GCB Bioenergy 11(5):672–690

    CAS  Google Scholar 

  16. 16.

    Daverdin G, Bahri BA, Wu XM, Serba DD, Tobias C, Saha MC, Devos KM (2015) Comparative relationships and chromosome evolution in switchgrass (Panicum virgatum) and its genomic model, foxtail millet ( Setaria italica). Bioenergy Research 8(1):137–151

    Google Scholar 

  17. 17.

    Serba D, Wu L, Daverdin G, Bahri BA, Wang X, Kilian A, Bouton JH, Brummer EC, Saha MC, Devos KM (2013) Linkage maps of lowland and upland tetraploid switchgrass ecotypes. Bioenergy Research 6(3):953–965

    Google Scholar 

  18. 18.

    Casler MD, Tobias CM, Kaeppler SM, Buell CR, Wang Z-Y, Cao P, Schmutz J, Ronald P (2011) The switchgrass genome tools and strategies. The Plant Genome 4(3):273–282

    CAS  Google Scholar 

  19. 19.

    Lipka AE, Lu F, Cherney JH, Buckler ES, Casler MD, Costich DE (2014) Accelerating the switchgrass (Panicum virgatum L.) breeding cycle using genomic selection approaches. PLoS One 9(11)

  20. 20.

    Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel insights from a network-based SNP discovery protocol. PLoS Genet 9:1

    Google Scholar 

  21. 21.

    Taylor M, Tornqvist CE, Zhao X, Grabowski P, Doerge R, Ma J, Volenec J, Evans J, Ramstein GP, Sanciangco MD, Buell CR, Casler MD, Jiang Y (2018) Genome-wide association study in pseudo-F populations of switchgrass identifies genetic loci affecting heading and anthesis dates. Front Plant Sci 9:1250. https://doi.org/10.3389/fpls.2018.01250

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Lin CY, Donohoe BS, Ahuja N, Garrity DM, Qu RD, Tucker MP, Himmel ME, Wei H (2017) Evaluation of parameters affecting switchgrass tissue culture: toward a consolidated procedure for Agrobacterium-mediated transformation of switchgrass (Panicum virgatum). Plant Methods 13:113. https://doi.org/10.1186/s13007-017-0263-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Merrick P, Fei SZ (2015) Plant regeneration and genetic transformation in switchgrass - a review. J Integr Agr 14(3):483–493

    CAS  Google Scholar 

  24. 24.

    Nelson RS, Stewart CN Jr, Gou J, Holladay S, Gallego-Giraldo L, Flanagan A, DGJ M, Hisano H, Wuddineh WA, Poovaiah CR, Srivastava A, Biswal AK, Shen H, Escamilla-Treviño LL, Yang J, Hardin CF, Nandakumar R, Fu C, Zhang J, Xiao X, Percifield R, Chen F, Bennetzen JL, Udvardi M, Mazarei M, Dixon RA, Wang ZY, Tang Y, Mohnen D, Davison BH (2017) Development and use of a switchgrass (Panicum virgatum L.) transformation pipeline by the BioEnergy Science Center to evaluate plants for reduced cell wall recalcitrance. Biotechnol biofuels 10:309. https://doi.org/10.1186/s13068-017-0991-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Lionetti V, Francocci F, Ferrari S, Volpi C, Bellincampi D, Galletti R, D'Ovidio R, De Lorenzo G, Cervone F (2010) Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc Natl Acad Sci U S A 107(2):616–621

    CAS  PubMed  Google Scholar 

  26. 26.

    Costa G, Plazanet I (2016) Plant cell wall, a challenge for its characterisation. Advances in Biological Chemistry 6(3):70–105

    CAS  Google Scholar 

  27. 27.

    Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11(3):266–277

    CAS  PubMed  Google Scholar 

  28. 28.

    Mohnen D, Bar-Peled L, Somerville C (2008) Cell wall synthesis. In: Himmel M (ed) Biomass recalcitrance: deconstruction the plant cell wall for bioenergy. Wiley-Blackwell, Oxford, pp 94–187

    Google Scholar 

  29. 29.

    Caffall KH, Pattathil S, Phillips SE, Hahn MG, Mohnen D (2009) Arabidopsis thaliana T-DNA mutants implicate GAUT genes in the biosynthesis of pectin and xylan in cell walls and seed testa. Mol Plant 2(5):1000–1014

    CAS  PubMed  Google Scholar 

  30. 30.

    Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546

    CAS  PubMed  Google Scholar 

  31. 31.

    Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH et al (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3:29–60

    CAS  Google Scholar 

  32. 32.

    Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344(14):1879–1900

    CAS  PubMed  Google Scholar 

  33. 33.

    D'Ovidio R, Mattei B, Roberti S, Bellincampi D (2004) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. BBA - Proteins and Proteomics 1696(2):237–244

    CAS  PubMed  Google Scholar 

  34. 34.

    Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5(3):224–229

    CAS  PubMed  Google Scholar 

  35. 35.

    Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P (2009) Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 60(6):974–982

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Lewis NG (1999) A 20th century roller coaster ride: a short account of lignification. Curr Opin Plant Biol 2(2):153–162

    CAS  PubMed  Google Scholar 

  37. 37.

    Ridley BL, O'Neill MA, Mohnen DA (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57(6):929–967

    CAS  PubMed  Google Scholar 

  38. 38.

    Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132(2):1033–1040

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Chen RQ, Zhang SZ, Sun SL, Chang JH, Zuo JR (2005) Characterization of a new mutant allele of the Arabidopsis Flowering locus D (FLD) gene that controls the flowering time by repressing FLC. Chin Sci Bull 50(23):2701–2706

    Google Scholar 

  40. 40.

    Francocci F, Bastianelli E, Lionetti V, Ferrari S, De Lorenzo G, Bellincampi D, Cervone F (2013) Analysis of pectin mutants and natural accessions of Arabidopsis highlights the impact of de-methyl-esterified homogalacturonan on tissue saccharification. Biotechnol Biofuels 6:163. https://doi.org/10.1186/1754-6834-6-163

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Ramos LP (2003) The chemistry involved in the steam treatment of lignocellulosic materials. Quim Nova 26(6):863–871

    CAS  Google Scholar 

  42. 42.

    Shadle G, Chen F, Reddy MSS, Jackson L, Nakashima J, Dixon RA (2007) Down-regulation of hydroxycinnamoyl CoA: Shikimate hydroxycinnamoyl transferase in transgenic Alfalfa affects lignification, development and forage quality. Phytochemistry 68(11):1521–1529

    CAS  PubMed  Google Scholar 

  43. 43.

    Dey S, Maiti TK, Bhattacharyya BC (1994) Production of some extracellular enzymes by a lignin peroxidase-producing brown-rot fungus, Polyporus ostreiformis, and its comparative abilities for lignin degradation and dye decolorization. Appl Environ Microbiol 60(11):4216–4218

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Kirk TK, Farrell RL (1987) Enzymatic combustion - the microbial-degradation of lignin. Annu Rev Microbiol 41:465–505

    CAS  PubMed  Google Scholar 

  45. 45.

    de Gonzalo G, Colpa DI, Habib MHM, Fraaije MW (2016) Bacterial enzymes involved in lignin degradation. J Biotechnol 236:110–119

    PubMed  Google Scholar 

  46. 46.

    Lambertz C, Ece S, Fischer R, Commandeur U (2016) Progress and obstacles in the production and application of recombinant lignin-degrading peroxidases. Bioengineered 7(3):145–154

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Min K, Gong G, Woo HM, Kim Y, Um Y (2015) A dye-decolorizing peroxidase from Bacillus subtilis exhibiting substrate-dependent optimum temperature for dyes and β-ether lignin dimer. Sci Rep 5:8245. https://doi.org/10.1038/srep08245

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Rahmanpour R, TDH B (2015) Characterisation of Dyp-type peroxidases from Pseudomonas fluorescens Pf-5 oxidation of Mn(II) and polymeric lignin by Dyp1B. Arch Biochem Biophys 574:93–98

    CAS  PubMed  Google Scholar 

  49. 49.

    Roberts JN, Singh R, Grigg JC, Murphy MEP, Bugg TDH, Eltis LD (2011) Characterization of dye-decolorizing peroxidases from Rhodococcus jostii RHA1. Biochemistry-Us 50(23):5108–5119

    CAS  Google Scholar 

  50. 50.

    Yu WN, Liu WN, Huang HQ, Zheng F, Wang XY, Wu YY, Li KJ, Xie XM, Jin Y (2014) Application of a novel alkali-tolerant thermostable dyP-type peroxidase from Saccharomonospora viridis DSM 43017 in biobleaching of eucalyptus Kraft pulp. PLoS One 9:10

    PubMed Central  Google Scholar 

  51. 51.

    Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28(12):1883–1896

    CAS  PubMed  Google Scholar 

  52. 52.

    Biz A, Farias FC, Motter FA, de Paula DH, Richard P, Krieger N, Mitchell DA (2014) Pectinase activity determination: an early deceleration in the release of reducing sugars throws a spanner in the works! PLoS One 9:10

    Google Scholar 

  53. 53.

    Collares RM, Miklasevicius LVS, Bassaco MM, Salau NPG, Mazutti MA, Bisognin DA, Terra LM (2012) Optimization of enzymatic hydrolysis of cassava to obtain fermentable sugars. J Zhejiang Univ-Sc B 13(7):579–586

    CAS  Google Scholar 

  54. 54.

    Hossain ABMS, Ahmed SA, Alshammari AM, Adnan FMA, Annuar MSM, Mustafa H, Hammad N (2011) Bioethanol fuel production from rotten banana as an environmental waste management and sustainable energy. Afr J Microbiol Res 5(6):586–598

    CAS  Google Scholar 

  55. 55.

    Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25(7):759–761

    CAS  PubMed  Google Scholar 

  56. 56.

    Dien BS, Sarath G, Pedersen JF, Sattler SE, Chen H, Funnell-Harris DL, Nichols NN, Cotta MA (2009) Improved sugar conversion and ethanol yield for forage sorghum (Sorghum bicolor L. Moench) lines with reduced lignin contents. Bioenergy Research 2(3):153–164

    Google Scholar 

  57. 57.

    Vermerris W, Saballos A, Ejeta G, Mosier NS, Ladisch MR, Carpita NC (2007) Molecular breeding to enhance ethanol production from corn and sorghum stover. Crop Sci 47:S142–S153

    Google Scholar 

  58. 58.

    Barriere Y, Guillet C, Goffner D, Pichon M (2003) Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Anim Res 52(3):193–228

    CAS  Google Scholar 

  59. 59.

    Guo DG, Chen F, Wheeler J, Winder J, Selman S, Peterson M, Dixon RA (2001) Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res 10(5):457–464

    CAS  PubMed  Google Scholar 

  60. 60.

    Jung HG, Allen MS (1995) Characteristics of plant-cell walls affecting intake and digestibility of forages by ruminants. J Anim Sci 73(9):2774–2790

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Bate NJ, Orr J, Ni WT, Meromi A, Nadlerhassar T, Doerner PW, Dixon RA, Lamb CJ, Elkind Y (1994) Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc Natl Acad Sci U S A 91(16):7608–7612

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19(1):148–162

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Capodicasa C, Vairo D, Zabotina O, McCartney L, Caprari C, Mattei B, Manfredini C, Aracri B, Benen J, Knox JP, de Lorenzo G, Cervone F (2004) Targeted modification of homogalacturonan by transgenic expression of a fungal polygalacturonase alters plant growth. Plant Physiol 135(3):1294–1304

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Eudes A, Pereira JH, Yogiswara S, Wang G, Benites VT, Baidoo EEK, Lee TS, Adams PD, Keasling JD, Loque D (2016) Exploiting the substrate promiscuity of hydroxycinnamoyl-CoA:shikimate hydroxycinnamoyl transferase to reduce lignin. Plant Cell Physiol 57(3):568–579

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C, Pollet B, Legrand M (2004) Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16(6):1446–1465

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17(8):808–812

    CAS  PubMed  Google Scholar 

  67. 67.

    Lapierre C, Pilate G, Pollet B, Mila I, Leple JC, Jouanin L, Kim H, Ralph J (2004) Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins. Phytochemistry 65(3):313–321

    CAS  PubMed  Google Scholar 

  68. 68.

    Li XJ, Yang Y, Yao JL, Chen GX, Li XH, Zhang QF, Wu CY (2009) FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Mol Biol 69(6):685–697

    CAS  PubMed  Google Scholar 

  69. 69.

    Park SH, Ong RG, Mei C, Sticklen M (2014) Lignin down-regulation of Zea mays via dsRNAi and klason lignin analysis. J Vis Exp 89:51340. https://doi.org/10.3791/51340

    CAS  Article  Google Scholar 

  70. 70.

    Piquemal J, Chamayou S, Nadaud I, Beckert M, Barriere Y, Mila I, Lapierre C, Rigau J, Puigdomenech P, Jauneau A et al (2002) Down-regulation of caffeic acid O-methyltransferase in maize revisited using a transgenic approach. Plant Physiol 130(4):1675–1685

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Zhang KW, Qian Q, Huang ZJ, Wang YQ, Li M, Hong LL, Zeng DL, Gu MH, Chu CC, Cheng ZK (2006) GOLD HULL and INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol 140(3):972–983

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54(4):569–581

    CAS  PubMed  Google Scholar 

  73. 73.

    Nakashima J, Chen F, Jackson L, Shadle G, Dixon RA (2008) Multi-site genetic modification of monolignol biosynthesis in alfalfa (Medicago sativa): effects on lignin composition in specific cell types. New Phytol 179(3):738–750

    CAS  PubMed  Google Scholar 

  74. 74.

    Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11(3):278–285

    CAS  PubMed  Google Scholar 

  75. 75.

    Raiola A, Camardella L, Giovane A, Mattei B, De Lorenzo G, Cervone F, Bellincampi D (2004) Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett 557(1–3):199–203

    CAS  PubMed  Google Scholar 

  76. 76.

    Mouille G, Ralet MC, Cavelier C, Eland C, Effroy D, Hematy K, McCartney L, Truong HN, Gaudon V, Thibault JF et al (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J 50(4):605–614

    CAS  PubMed  Google Scholar 

  77. 77.

    Raiola A, Lionetti V, Elmaghraby I, Immerzeel P, Mellerowicz EJ, Salvi G, Cervone F, Bellincampi D (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe In 24(4):432–440

    CAS  Google Scholar 

  78. 78.

    Zeng YN, Zhao S, Yang SH, Ding SY (2014) Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Curr Opin Biotech 27:38–45

    CAS  PubMed  Google Scholar 

  79. 79.

    Lalitha S (2000) Primer premier 5.0. Biotech Software and Internet Report 1(6):270–272

    Google Scholar 

  80. 80.

    Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15

    Google Scholar 

  81. 81.

    Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:3

    Google Scholar 

  82. 82.

    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data P (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    PubMed  PubMed Central  Google Scholar 

  83. 83.

    McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28(19):2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14(8):2611–2620

    CAS  PubMed  Google Scholar 

  87. 87.

    Earl DA, vonHoldt BM: Structure harvester (2012) A website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

    Google Scholar 

  88. 88.

    Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73(5):1162–1169

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Salzburger W, Ewing GB, von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20(9):1952–1963

    PubMed  Google Scholar 

  90. 90.

    Moore JE, Brant MH, Kunkle WE, Hopkins DI (1999) Effects of supplementation on voluntary forage intake, diet digestibility, and animal performance. J Anim Sci 77:122–135

    CAS  PubMed  Google Scholar 

  91. 91.

    Moore JE, Undersander DJ (2002) Relative Forage Quality: An alternative to relative feed value and quality index. p. 16-31 In: Proc. Florida Ruminant Nutrition Symposium, January 10-11, University of Florida, Gainesville

  92. 92.

    NRC (2001) Nutrient requirements of dairy cattle, 7th rev. edn. Natl. Acad. Sci, Washington

    Google Scholar 

  93. 93.

    R Core Team: R (2004) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org/

    Google Scholar 

  94. 94.

    Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635

    CAS  PubMed  Google Scholar 

  95. 95.

    Casler MD, Vogel KP, Taliaferro CM, Ehlke NJ, Berdahl JD, Brummer EC, Kallenbach RL, West CP, Mitchell RB (2007) Latitudinal and longitudinal adaptation of switchgrass populations. Crop Sci 47(6):2249–2260

    Google Scholar 

  96. 96.

    Gunter LE, Tuskan GA, Wullschleger SD (1996) Diversity among populations of switchgrass based on RAPD markers. Crop Sci 36(4):1017–1022

    Google Scholar 

  97. 97.

    Acharya AR (2014) Genetic diversity, population structure and association mapping of biofuel traits in southern switchgrass germplasm. PhD dissertation, 130p, University of Gerogia https://getd.libs.uga.edu/pdfs/acharya_ananta_r_201408_phd.pdf. Accessed Jan 2017

  98. 98.

    Grabowski PP, Evans J, Daum C, Deshpande S, Barry KW, Kennedy M, Ramstein G, Kaeppler SM, Buell CR, Jiang Y et al (2016) Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data. New Phytol 213:1

    Google Scholar 

  99. 99.

    Casler MD, Vogel KP, Taliaferro CM, Wynia RL (2004) Latitudinal adaptation of switchgrass populations. Crop Sci 44(1):293–303

    Google Scholar 

  100. 100.

    McMillan C (1959) The role of ecotypic variation in the distribution of the central grassland of North America. Ecol Monogr 29(4):285–308

    Google Scholar 

  101. 101.

    McMillan C (1965) Ecotypic differentiation within 4 north American prairie grasses. 2. Behavioral varaition within transplanted community fractions. American journal of botany 52(1):55

    Google Scholar 

  102. 102.

    Zhang Y, Zalapa J, Jakubowski AR, Price DL, Acharya A, Wei Y, Brummer EC, Kaeppler SM, Casler MD (2011) Natural hybrids and gene flow between upland and lowland switchgrass. Crop Sci 51(6):2626–2641

    Google Scholar 

  103. 103.

    Bartley L, Wu GA, Wu Y, Rokhsar DS, Schmutz J, Saha MC, Barry KW, Thibivilliers S, Juenger T, Lowry D et al (2016) Expected and unexpected patterns of chromosomal inheritance from resequencing of tetraploid switchgrass. Plant and Animal Genome Conference XXIV January 9–13, 2016 San Diego, CA Poster W673

  104. 104.

    Missaoui AM, Paterson AH, Bouton JH (2005) Investigation of genomic organization in switchgrass (Panicum virgatum L.) using DNA markers. Theor Appl Genet 110(8):1372–1383

    CAS  PubMed  Google Scholar 

  105. 105.

    Tobias CM, Sarath G, Twigg P, Lindquist E, Pangilinan J, Penning BW, Barry K, McCann MC, Carpita NC, Lazo GR (2008) Comparative genomics in switchgrass using 61,585 high-quality expressed sequence tags. Plant Genome 1(2):111–124

    CAS  Google Scholar 

  106. 106.

    Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135(1):254–265

    CAS  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, Pean M, Danoun S, Halpin C, Grima-Pettenati J, Boudet AM (2001) Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. Plant J 28(3):257–270

    CAS  PubMed  Google Scholar 

  108. 108.

    Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C (2002) Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J 30(1):47–59

    CAS  PubMed  Google Scholar 

  109. 109.

    Brenner EA, Zein I, Chen YS, Andersen JR, Wenzel G, Ouzunova M, Eder J, Darnhofer B, Frei U, Barriere Y, Lübberstedt T (2010) Polymorphisms in Omethyltransferase genes are associated with Stover cell wall digestibility in European maize (Zea mays L.). BMC Plant Biol 10:27. https://doi.org/10.1186/1471-2229-10-27

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Huhtanen P, Rinne M, Nousiainen J (2009) A meta-analysis of feed digestion in dairy cows. 2. The effects of feeding level and diet composition on digestibility. J Dairy Sci 92(10):5031–5042

    CAS  PubMed  Google Scholar 

  111. 111.

    Bhandari HS, Nayak S, Dalid CO, Sykes VR (2007) Biomass yield heterosis in lowland switchgrass. Crop Sci 57(4):2015–2023

    Google Scholar 

  112. 112.

    Martinez-Reyna JM, Vogel KP (2002) Incompatibility systems in switchgrass. Crop Sci 42(6):1800–1805

    Google Scholar 

  113. 113.

    Martinez-Reyna JM, Vogel KP (2008) Heterosis in switchgrass: spaced plants. Crop Sci 48(4):1312–1320

    Google Scholar 

Download references

Funding

This project was achieved with funding provided by The BioEnergy Science Center and The Center for Bioenergy Innovation, U.S. Department of Energy Research Centers supported by the Office of Biological and Environmental Research in the DOE Office of Science.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Bochra A. Bahri.

Ethics declarations

Conflict of Interests

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(XLSX 94 kb)

ESM 2

(DOCX 714 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bahri, B.A., Daverdin, G., Xu, X. et al. Natural Variation in Lignin and Pectin Biosynthesis-Related Genes in Switchgrass (Panicum virgatum L.) and Association of SNP Variants with Dry Matter Traits. Bioenerg. Res. 13, 79–99 (2020). https://doi.org/10.1007/s12155-020-10090-2

Download citation

Keywords

  • Single nucleotide polymorphisms (SNPs)
  • Population structure
  • Evolution
  • Heterosis
  • Dry matter
  • Association analysis