Skip to main content

Advertisement

Log in

Exploring Flowering Genes in Isabgol (Plantago ovata Forsk.) Through Transcriptome Analysis

  • Original Article
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Background

Flowering is one of the major developmental processes that govern the economic yield of crop plants. However, little is known about the molecular mechanisms underlying flowering in Isabgol, an important high-value medicinal crop. Here, we analyzed the leaf transcriptome of early and late flowering genotypes by high throughput next-generation sequencing to uncover the genes and pathways involved in flowering time and flower development.

Results

Illumina paired-end sequencing of Isabgol leaves at the stem elongation stage, generated 8,976,119 and 4,282,684 reads respectively in DPO-14 (early flowering) and DPO-185 (late flowering) genotypes. The sequence assembly resulted in 40,175 and 39,533 transcripts respectively in early and late genotypes. A total of 17,768 (95.50) in DPO-14 and 21,255 (94.10) in DPO-185 CDS were annotated. There were 8981CDS were differentially expressed of which 1220 (13.58%) were significantly upregulated while 1485 (16.53%) CDS were significantly downregulated in DPO-185 compared with DPO-14. In total, 229 genes were identified belongs to distinct flowering pathways in Isabgol. A putative schematic network of flowering pathway regulation in Isabgol was proposed. Significant DEGs (60 genes) related to flowering time and flower development were detected between the early and late flowering genotypes. Significant differences in fold change expression of 17 genes were observed in early and late flowering genotypes.

Conclusion

Many differentially expressed genes (DEGs) involved in flowering time and flower development were identified. The expression data will serve as a resource for unraveling the functions of specific genes involved in flower development in Isabgol and other plants. These findings are significant for further understanding of the molecular basis for flowering time regulation, breeding, and molecular biology in Isabgol as well as other crop plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The datasets supporting the results of this article are available at the National Center for Biotechnology Information (NCBI) BioProject database (Short Read Archive) under accession number PRJNA382334 and the Transcriptome Shotgun Assembly (TSA) at DDBJ/EMBL/GenBank under the accession GFNS00000000. The version described in this paper is the first version, GFNS00000000.

References

  • Abe M, Kaya H, Watanabe-Taneda A (2015) FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1. Plant J 83:1059–1068

    Article  CAS  PubMed  Google Scholar 

  • Abou-Elwafa SF, Büttner B, Chia T (2011) Conservation and divergence of autonomous pathway genes in the flowering regulatory network of Beta vulgaris. J Exp Bot 62:3359–3374

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Auge GA, Blair LK, Karediya A, Donohue K (2018) The autonomous flowering-time pathway pleiotropically regulates seed germination in Arabidopsis thaliana. Ann Bot 121:183–191

    Article  CAS  PubMed  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and lts APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avila de Dios E, Delaye L, Simpson J (2019) Transcriptome analysis of bolting in A. tequilana reveals roles for florigen, MADS, fructans and gibberellins. BMC Genomics 20:473

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Balasubramanian S, Weigel D (2006) Temperature induced flowering in Arabidopsis thaliana. Plant Signal Behav 1(5):227–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Basu U, Narnoliya L, Srivastava R (2019) CLAVATA signaling pathway genes modulating flowering time and flower number in chickpea. Theor Appl Genet 132:2017–2038

    Article  CAS  PubMed  Google Scholar 

  • Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    Article  PubMed  CAS  Google Scholar 

  • Bendix C, Marshall CM, Harmon FG (2015) Circadian clock genes universally control key agricultural traits. Mol Plant 8:1135–1152

    Article  CAS  PubMed  Google Scholar 

  • Biassoni R, Raso (2014) A quantitative real-time PCR methods and protocols methods in molecular biology:1160

  • Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops-what did we learn from arabidopsis? Curr Opin Biotechnol 32:121–129

    Article  PubMed  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouché F, Lobet G, Tocquin P, Périlleux C (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44:D1167–D1171

    Article  PubMed  CAS  Google Scholar 

  • Campoli C, Pankin A, Drosse B (2013) HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways. New Phytol 199:1045–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos-Rivero G, Osorio-Montalvo P, Sánchez-Borges R (2017) Plant hormone signaling in flowering: an epigenetic point of view. J Plant Physiol 214:16–27

    Article  CAS  PubMed  Google Scholar 

  • Capovilla G, Schmid M, Posé D (2015) Control of flowering by ambient temperature. J Exp Bot 66:59–69

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Qi S, Zhang D (2018) Comparative RNA-sequencing-based transcriptome profiling of buds from profusely flowering “Qinguan” and weakly flowering “Nagafu no. 2” apple varieties reveals novel insights into the regulatory mechanisms underlying floral induction. BMC Plant Biol 18

  • Cheng JZ, Zhou YP, Lv TX (2017) Research progress on the autonomous flowering time pathway in arabidopsis. Physiol Mol Biol Plants 23:477–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719

    Article  CAS  PubMed  Google Scholar 

  • Cho LH, Pasriga R, Yoon J (2018) Roles of sugars in controlling flowering time. J. Plant Biol. 61:121–130

    Article  CAS  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  CAS  PubMed  Google Scholar 

  • Conti L (2017) Hormonal control of the floral transition: can one catch them all? Dev Biol 430:288–301

    Article  CAS  PubMed  Google Scholar 

  • Creux N, Harmer S (2019) Circadian rhythms in plants. Cold Spring Harb Perspect Biol 11

  • Dhar MK, Kaul S, Sharma P, Gupta M (2011) Plantago ovata : cultivation, genomics, chemistry and therapeutic applications. In: Singh RJ (ed) Genetic resources, chromosome engineering and crop improvement. CRC Press, New York, USA

    Google Scholar 

  • Digel B, Pankin A, von Korff M (2015) Global transcriptome profiling of developing leaf and shoot apices reveals distinct genetic and environmental control of floral transition and inflorescence development in barley. Plant Cell 27:2318–2334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding J, Nilsson O (2016) Molecular regulation of phenology in trees-because the seasons they are a-changin. Curr Opin Plant Biol 29:73–79

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184

    Article  CAS  PubMed  Google Scholar 

  • Dong Z, Danilevskaya O, Abadie T (2012) A gene regulatory network model for floral transition of the shoot apex in maize and its dynamic modeling. PLoS One 7:e43450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duncan S, Holm S, Questa J (2015) Seasonal shift in timing of vernalization as an adaptation to extreme winter. Elife 4

  • Eom H, Park SJ, Kim MK (2018) TAF15b, involved in the autonomous pathway for flowering, represses transcription of FLOWERING LOCUS C. Plant J 93:79–91

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Zhao Y, Wang K (2016) Identification of vernalization responsive genes in the winter wheat cultivar Jing841 by transcriptome sequencing. J Genet 95:957–964

    Article  CAS  PubMed  Google Scholar 

  • Feng G, Huang L, Li J (2017) Comprehensive transcriptome analysis reveals distinct regulatory programs during vernalization and floral bud development of orchardgrass (Dactylis glomerata L.). BMC Plant Biol 17

  • Finkelstein RR, Zeevaart J (1994) Gibberellin and abscisic acid biosynthesis and response. In: Somerville CR, Meyerowitz EM (eds) Arabidopsis. Cold Spring Harbor, NY, Cold Spring Harbor Laboratoty Press, pp 523–553

    Google Scholar 

  • Fornara F, Panigrahi KCS, Gissot L (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86

    Article  CAS  PubMed  Google Scholar 

  • Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141(3):550

    Article  PubMed  Google Scholar 

  • Gawroński P, Ariyadasa R, Himmelbach A (2014) A distorted circadian clock causes early flowering and temperature-dependent variation in spike development in the Eps-3Am mutant of einkorn wheat. Genetics 196:1253–1261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghangal R, Chaudhary S, Jain M (2013) Optimization of de novo short read assembly of seabuckthorn (Hippophae rhamnoides L) transcriptome. PLoS One 8

  • Grabherr MG, Haas BJ, Yassour M (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimplet J, Tello J, Laguna N, Ibáñez J (2017) Differences in flower transcriptome between grapevine clones are related to their cluster compactness, fruitfulness, and berry size. Front Plant Sci 8

  • Gul H, Tong Z, Han X (2019) Comparative transcriptome analysis between ornamental apple species provides insights into mechanism of double flowering. Agronomy 9

  • Haas BJ, Papanicolaou A, Yassour M (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Haider (2014) Exploring flowering gene networks in soybean and arabidopsis through transcriptome analysis. PhD thesis Graduate College, University of Illinois at Urbana-Champaign, Illinois, USA

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hazen SP, Schultz TF, Pruneda-Paz JL (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci U S A 102:10387–10392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He W, Chen Y, Gao M (2018) Transcriptome analysis of Litsea cubeba floral buds reveals the role of hormones and transcription factors in the differentiation process. G3 Genes Genomes, Genet 8:1103–1114

    CAS  Google Scholar 

  • Helfer A, Nusinow DA, Chow BY (2011) LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21:126–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hennig L, Bouveret R, Gruissem W (2005) MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15:295–302

    Article  CAS  PubMed  Google Scholar 

  • Higgins JA, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using brachypodium distachyon as a model for the temperate grasses. PLoS One 5:e10065

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hill CB, Li C (2016) Genetic architecture of flowering phenology in cereals and opportunities for crop improvement. Front Plant Sci 7

  • Hou X, Guo Q, Wei W (2018) Screening of genes related to early and late flowering in tree peony based on bulked segregant RNA sequencing and verification by quantitative real-time PCR. Molecules 23

  • Huang H, Nusinow DA (2016) Into the evening: complex interactions in the arabidopsis circadian clock. Trends Genet 32:674–686

    Article  CAS  PubMed  Google Scholar 

  • Huang JZ, Lin CP, Cheng TC (2016) The genome and transcriptome of Phalaenopsis yield insights into floral organ development and flowering regulation. PeerJ 2016

  • Hudson KA (2010) The circadian clock-controlled transcriptome of developing soybean seeds 3

  • Hyun Y, Richter R, Coupland G (2017) Competence to flower: age-controlled sensitivity to environmental cues. Plant Physiol 173:36–46

    Article  CAS  PubMed  Google Scholar 

  • Imaizumi T, Kay SA (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558

    Article  CAS  PubMed  Google Scholar 

  • Janakiram T, Nagaraja Reddy R, Manivel P, Satyajit Roy (2019) Road map for Isabgol promotion in India, ICAR-Directorate of Medicinal and Aromatic Plants Research, Anand, Gujarat. 50pp

  • Jensen JK, Johnson N, Wilkerson CG (2013) Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue. Front Plant Sci:4–183

  • Johansson M, Staiger D (2015) Time to flower: interplay between photoperiod and the circadian clock. J Exp Bot 66:719–730

    Article  CAS  PubMed  Google Scholar 

  • Jones MA (2009) Entrainment of the arabidopsis circadian clock. J. Plant Biol. 52:202–209

    Article  CAS  Google Scholar 

  • Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19(9):2736–2748

  • Jung CH, Wong CE, Singh MB, Bhalla PL (2012) Comparative genomic analysis of soybean flowering genes. PLoS One 7

  • Jung WY, Park HJ, Lee A (2016) Identification of flowering-related genes responsible for differences in bolting time between two radish inbred lines. Front Plant Sci 7

  • Kikuchi R, Handa H (2009) Photoperiodic control of flowering in barley. Breed Sci 59:546–552

    Article  CAS  Google Scholar 

  • Kim D-H, Sung S (2014) Genetic and epigenetic mechanisms underlying vernalization. Arab B 12:e0171

    Article  Google Scholar 

  • Klepikova AV, Logacheva MD, Dmitriev SE, Penin AA (2015) RNA-seq analysis of an apical meristem time series reveals a critical point in Arabidopsis thaliana flower initiation. BMC Genomics 16:466

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Korves TM, Bergelson J (2003) A developmental response to pathogen infection in Arabidopsis. Plant Physiol 133:339–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotwal S, Kaul S, Sharma P (2016) De novo transcriptome analysis of medicinally important plantago ovata using RNA-seq. PLoS One 11:e0150273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807

    Article  CAS  PubMed  Google Scholar 

  • Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Amasino RM (2013) Two FLX family members are non-redundantly required to establish the vernalization requirement in arabidopsis. Nat Commun 4

  • Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254

    Article  CAS  PubMed  Google Scholar 

  • Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. Arab B 9:e0148

    Article  Google Scholar 

  • Li L, Li X, Liu Y, Liu H (2016) Flowering responses to light and temperature. Sci China Life Sci 59(4):403–408

  • Li W, Zhang L, Ding Z (2017) De novo sequencing and comparative transcriptome analysis of the male and hermaphroditic flowers provide insights into the regulation of flower formation in andromonoecious Taihangia rupestris. BMC Plant Biol 17:54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Y, Zhang D, An N (2019) Transcriptomic analysis reveals the regulatory module of apple (Malus × domestica) floral transition in response to 6-BA. BMC Plant Biol 19

  • Liew LC, Hecht V, Sussmilch FC, Weller JL (2014) The pea photoperiod response gene STERILE NODES is an ortholog of LUX ARRHYTHMO. Plant Physiol 165:648–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin YL, Tsay YF (2017) Influence of differing nitrate and nitrogen availability on flowering control in Arabidopsis. J Exp Bot 68:2603–2609

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Zhu Y, Shen L, Yu H (2013) Emerging insights into florigen transport. Curr Opin Plant Biol 16:607–613

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Sun M, Du D (2015) Whole-transcriptome analysis of differentially expressed genes in the vegetative buds, floral buds and buds of Chrysanthemum morifolium. PLoS One 10

  • Liu H, Sun M, Du D (2016) Whole-transcriptome analysis of differentially expressed genes in the ray florets and disc florets of Chrysanthemum morifolium. BMC Genomics 17

  • Liu C, Wang S, Xu W, Liu X (2017) Genome-wide transcriptome profiling of radish (Raphanus sativus L.) in response to vernalization. PLoS One 12

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Logacheva MD, Kasianov AS, Vinogradov DV (2011) De novo sequencing and characterization of floral transcriptome in two species of buckwheat (Fagopyrum). BMC Genomics 12:30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lulin H, Xiao Y, Pei S (2012) The first Illumina-based de novo transcriptome sequencing and analysis of safflower flowers. PLoS One 7

  • Lyons R, Rusu A, Stiller J (2015) Investigating the association between flowering time and defense in the Arabidopsis thaliana-Fusarium oxysporum interaction. PLoS One 10:e0127699

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manivel P, Raju S (2012) DPO14-an early maturating Isabgol (Plantago ovata Forsk) mutant. Indian Journal of Genetics and Plant Breeding 72:489–490

    Google Scholar 

  • Manivel P, Jincy M, Patel S, Jitendra K, Reddy NRR (2019) Comparative transcriptome analysis uncovers genes and pathways relating to host-plant resistance against downy mildew disease of Isabgol (Plantago ovata Forsk.). Functional and Integrative genomics (Communicated)

  • Marquardt S, Boss PK, Hadfield J, Dean C (2006) Additional targets of the Arabidopsis autonomous pathway members, FCA and FY. J Exp Bot 57:3379–3386

    Article  CAS  PubMed  Google Scholar 

  • Mehta RH, Ponnuchamy M, Kumar J, Reddy NRR (2017) Exploring drought stress-regulated genes in senna (Cassia angustifolia Vahl.): a transcriptomic approach. Funct Integr Genomics 17

  • Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46:292–299

    Article  CAS  PubMed  Google Scholar 

  • Morris WL, Hancock RD, Ducreux LJM (2014) Day length dependent restructuring of the leaf transcriptome and metabolome in potato genotypes with contrasting tuberization phenotypes. Plant Cell Environ 37:1351–1363

    Article  CAS  PubMed  Google Scholar 

  • Mouhu K, Hytönen T, Folta K, Rantanen M, Paulin L, Auvinen P, Elomaa P (2009) Identification of flowering genes in strawberry, a perennial SD plant. BMC Plant Biol 9:122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mutasa-Göttgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989

    Article  PubMed  CAS  Google Scholar 

  • Mutasa-Göttgens ES, Joshi A, Holmes HF (2012) A new RNASeq-based reference transcriptome for sugar beet and its application in transcriptome-scale analysis of vernalization and gibberellin responses. BMC Genomics:13

  • Nie S, Li C, Xu L (2016) De novo transcriptome analysis in radish (Raphanus sativus L.) and identification of critical genes involved in bolting and flowering. BMC Genomics 17

  • Nishiura A, Kitagawa S, Matsumura M (2018) An early-flowering einkorn wheat mutant with deletions of PHYTOCLOCK 1/LUX ARRHYTHMO and VERNALIZATION 2 exhibits a high level of VERNALIZATION 1 expression induced by vernalization. J Plant Physiol 222:28–38

    Article  CAS  PubMed  Google Scholar 

  • Ogiso E, Takahashi Y, Sasaki T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada R, Nemoto Y, Endo-Higashi N, Izawa T (2017) Synthetic control of flowering in rice independent of the cultivation environment. Nat Plants 3

  • Parcy F (2005) Flowering: a time for integration. Int J Dev Biol 49:585–593

    Article  PubMed  Google Scholar 

  • Park HJ, Kim WY, Pardo JM, Yun DJ (2016) Molecular interactions between flowering time and abiotic stress pathways. In: International Review of Cell and Molecular Biology. Elsevier Inc., pp 371–412

  • Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science (80- ) 330:1397–1400

    Article  CAS  Google Scholar 

  • Pommerrenig B, Barth I, Niedermeier M, Kapp S, Schmid J, Dwyer RA (2006) Common plantain. A collection of expressed sequence tags from vascular tissue and a simple and efficient transformation method. Plant Physiol 142:1427–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pommerrenig B, Feussner K, Zierer W, Rabinovych V, Kleb F, Feussner I (2011) Phloem-specific expression of Yang cycle genes and identification of novel Yang cycle enzymes in Plantago and Arabidopsis. Plant Cell 23:1904–1919

  • Reddy RNR, Madhusudhana R, Murali Mohan S, Chakravarthi DVN, Mehtre SP, Seetharama N (2013) Mapping QTL for grain yield and other agronomic traits in post-rainy sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 126:1921–1939

    Article  CAS  Google Scholar 

  • Reddy RNR, Mehta RH, Soni PH, Makasana J, Gajbhiye NA, Ponnuchamy M (2015) Next generation sequencing and transcriptome analysis predicts biosynthetic pathway of sennosides from senna (Cassia angustifolia Vahl.), a non-model plant with potent laxative properties. PLoS One 10

  • Ren L, Liu T, Cheng Y, Sun J, Gao J, Dong B (2016) Transcriptomic analysis of differentially expressed genes in the floral transition of the summer flowering chrysanthemum. BMC Genomics 17

  • Sarma KS (1983) Development physiology of Plantago ovata forsk under the influence of vernalization and photoperiods. PhD Theisis, Gujarat University, Ahmedabad http://hdl.handle.net/10603/30508

  • Seo E, Lee H, Jeon J, Park H, Kim J, Noh YS (2009) Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21:3185–3197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Ryu J, Kang SK, Park CM (2011) Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. Plant J 65:418–429

    Article  CAS  PubMed  Google Scholar 

  • Shah S, Weinholdt C, Jedrusik N, Molina C, Zou J, Große I (2018) Whole-transcriptome analysis reveals genetic factors underlying flowering time regulation in rapeseed (Brassica napus L.). Plant Cell Environ 41:1935–1947

    Article  CAS  PubMed  Google Scholar 

  • Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shim JS, Imaizumi T (2015) Circadian clock and photoperiodic response in arabidopsis: from seasonal flowering to redox homeostasis. Biochemistry 54:157–170

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Yang W (2017) E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol 58:1461–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shu K, Luo X, Meng Y, Yang W (2018) Toward a molecular understanding of abscisic acid actions in floral transition. Plant Cell Physiol 59:215–221

    Article  CAS  PubMed  Google Scholar 

  • Silverstone AL, Mak PYA, Martinez EC, Sun T (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146

  • Simpson GG (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of arabidopsis flowering time. Curr Opin Plant Biol 7:570–574

    Article  CAS  PubMed  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science (80-. ) 296:285–289

    Article  CAS  Google Scholar 

  • Simpson GG, Dijkwel PP, Quesada V (2003) FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113:777–787

    Article  CAS  PubMed  Google Scholar 

  • Singh VK, Jain M (2014) Transcriptome profiling for discovery of genes involved in shoot apical meristem and flower development. Genomics Data 2:135–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701

    Article  CAS  PubMed  Google Scholar 

  • Song YH, Lee I, Lee SY, Imaizumi T, Hong JC (2012) CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in arabidopsis. Plant J 69:332–342

    Article  CAS  PubMed  Google Scholar 

  • Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464

    Article  CAS  PubMed  Google Scholar 

  • Song K, Kim HC, Shin S, Kim KH, Moon JC, Kim JY (2017) Transcriptome analysis of flowering time genes under drought stress in maize leaves. Front Plant Sci 8

  • Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037

    Article  CAS  PubMed  Google Scholar 

  • Strange A, Li P, Lister C, Anderson J, Warthmann N, Shindo C (2011) Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLoS One 6:e19949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Sugano S, Andronis C, Ong MS, Green RM, Tobin EM (1999) The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc Natl Acad Sci U S A 96:12362–12366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun M, Qi X, Hou L, Xu X, Zhu Z, Li M (2015) Gene expression analysis of Pak choi in response to vernalization. PLoS One 10

  • Sun Y, Wang G, Li Y (2016) De novo transcriptome sequencing and comparative analysis to discover genes related to floral development in Cymbidium faberi Rolfe Springerplus 5

  • Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the α subunit of protein kinase CK2. Proc Natl Acad Sci U S A 98:7922–7927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeno K (2016) Stress-induced flowering: the third category of flowering response. J Exp Bot 67:4925–4934

    Article  CAS  PubMed  Google Scholar 

  • Tao X, Gu YH, Jiang YS, Zhang YZ, Wang HY (2013) Transcriptome analysis to identify putative floral-specific genes and flowering regulatory-related genes of sweet potato. Biosci Biotechnol Biochem 77:2169–2174

    Article  CAS  PubMed  Google Scholar 

  • Teotia S, Tang G (2015) To bloom or not to bloom: role of micro RNAs in plant flowering. Mol Plant 8:359–377

    Article  CAS  PubMed  Google Scholar 

  • Tognetti JA, Pontis HG, Martínez-Noël GMA (2013) Sucrose signaling in plants: a world yet to be explored. Plant Signal Behav 8:e23316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

    Article  CAS  PubMed  Google Scholar 

  • Tsuji H, Taoka KI, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52

    Article  CAS  PubMed  Google Scholar 

  • Turck F, Fornara F, Coupland G (2008) Regulation and identity of Florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Dijk ADJ, Molenaar J (2017) Floral pathway integrator gene expression mediates gradual transmission of environmental and endogenous cues to flowering time. PeerJ 2017

  • Vining KJ, Romanel E, Jones RC, Klocko A, Alves-Ferreira M, Hefer CA (2015) The floral transcriptome of Eucalyptus grandis. New Phytol 206:1406–1422

    Article  CAS  PubMed  Google Scholar 

  • Wagner GP, Kin K, Lynch VJ (2012) Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci 131:281–285

    Article  CAS  PubMed  Google Scholar 

  • Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science (80- ) 339:704–707

    Article  CAS  Google Scholar 

  • Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4723–4730

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Köhler C (2017) Epigenetic processes in flowering plant reproduction. J Exp Bot 68:797–807

    CAS  PubMed  Google Scholar 

  • Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164–e164

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang S, Li Z, Jin W, Fang Y, Yang Q, Xiang J (2018) Transcriptome analysis and identification of genes associated with flower development in Rhododendron pulchrum sweet (Ericaceae). Gene 679:108–118

    Article  CAS  PubMed  Google Scholar 

  • Wen Z, Guo W, Li J, Lin H, He C, Liu Y (2017) Comparative transcriptomic analysis of vernalization- A nd cytokinin-induced floral transition in Dendrobium nobile. Sci Rep 7

  • Werner JD, Borevitz JO, Warthmann N, Trainer GT, Ecker JR, Chory J (2005) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc Natl Acad Sci U S A 102:2460–2465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wollenberg AC, Strasser B, Cerdán PD, Amasino RM (2008) Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between flowering locus C-mediated repression and photoperiodic induction of flowering. Plant Physiol 148:1681–1694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miRr156 and its target SPL3. Development 133:3539–3547

    Article  CAS  PubMed  Google Scholar 

  • Xiao M, Zhang Y, Chen X, Lee EJ, Barber CJS, Chakrabarty R (2013) Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J Biotechnol 166:122–134

    Article  CAS  PubMed  Google Scholar 

  • Yaish MW, Colasanti J, Rothstein SJ (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62:3727–3735

    Article  CAS  PubMed  Google Scholar 

  • Yan Z, Liang D, Liu H, Zheng G (2010) FLC: a key regulator of flowering time in arabidopsis. Russ J Plant Physiol 57:166–174

    Article  CAS  Google Scholar 

  • Yang S, Sun X, Jiang X (2019) Characterization of the Tibet plateau Jerusalem artichoke (Helianthus tuberosus L.) transcriptome by de novo assembly to discover genes associated with fructan synthesis and SSR analysis. Hereditas 156:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yongfeng W, Aiquan Z, Fengli S, Mao L, Kaijie X, Chao Z (2018) Using transcriptome analysis to identify genes involved in switchgrass flower reversion. Front Plant Sci 871

  • Yu S, Cao L, Zhou C-M, Zhang T-Q, Lian H, Sun Y (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants 2:269

    Google Scholar 

  • Yue J, Zhu C, Zhou Y (2018) Transcriptome analysis of differentially expressed unigenes involved in flavonoid biosynthesis during flower development of Chrysanthemum morifolium ‘Chuju’. Sci Rep 8

  • Zeng F, Biligetu B, Coulman B, Schellenberg MP, Fu YB (2017) RNA-Seq analysis of gene expression for floral development in crested wheatgrass (Agropyron cristatum L.). PLoS One:12

  • Zeng X, Liu H, Du H, Wang S, Yang W, Chi Y (2018) Soybean MADS-box gene GmAGL1 promotes flowering via the photoperiod pathway. BMC Genomics 19:51

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang J, Wu K, Zeng S, Teixeira da Silva JA, Zhao X, Tian CE (2013) Transcriptome analysis of Cymbidium sinense and its application to the identification of genes associated with floral development. BMC Genomics 14

  • Zhang L, Wang L, Yang Y, Cui J, Chang F, Wang Y (2015) Analysis of Arabidopsis floral transcriptome: detection of new florally expressed genes and expansion of Brassicaceae-specific gene families. Front Plant Sci 5:1–9

    Google Scholar 

  • Zhu L, Zhang Y, Guo W (2014) De novo assembly and characterization of Sophora japonica transcriptome using RNA-seq. Biomed Res Int 2014

  • Zografos BR, Sung S (2012) Vernalization-mediated chromatin changes. J Exp Bot 63:4343–4348

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the Director, ICAR-Directorate of Medicinal and Aromatic Plants Research, Boriavi, Anand, Gujarat, India, and Indian Council of Agricultural research (ICAR), New Delhi, for the facilities to undertake the study.

Funding

The authors gratefully acknowledge the Department of Science and Technology (DST), Government of India (GOI) for financially supporting this work under SERB/EMR/2014/000317 and SERB/EEQ/2016/000693.

Author information

Authors and Affiliations

Authors

Contributions

Conceived and designed the experiments: NRRR, MP. Performed the experiments: AP, KP, RG, NRRR MP. Analyzed the data: SP, NRRR MP JK, RRP. Contributed reagents/materials/analysis tools: NRRR MP JK. Wrote the paper: NRRR MP RRP.

Corresponding author

Correspondence to Nagaraja Reddy Rama Reddy.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Additional information

Publisher’s Note

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

Key Message

Flowering affects the yield and quality of crop plants. In this study, leaf transcriptome sequencing of early and late flowering genotypes has led to identification of 229 genes that belong to flowering time and flower developmental pathways in Isabgol. A schematic network of flowering pathway regulation in Isabgol was proposed.

Electronic Supplementary Materials

Supplementary Figure 1

Flowering pathways in Isabgol (Plantago ovata Forsk.). Adopted from https://www.wikipathways.org/index.php/Pathway:WP2312 (PDF 836 kb)

Additional file S1

Functional annotation of coding DNA sequences predicted in the leaf transcriptome of Isabgol (Plantago ovata Forsk.) (XLS 6115 kb)

Additional file S2

Differentially expressed genes (DEGs) identified in the leaf transcriptome of DPO-185 and DPO-14 genotypes of Isabgol (Plantago ovata Forsk.) (XLS 5624 kb)

Additional file S3

Flowering genes in the leaf transcriptome of Isabgol (Plantago ovata Forsk.) (XLSX 94 kb)

Additional file S4

ANOVA for the gene expression in fold change in early and late genotypes of Isabgol (Plantago ovata Forsk.) (DOCX 17 kb)

Additional file S5

GO ontology of significantly deferentially expressed genes in the leaf transcriptome of Isabgol (Plantago ovata Forsk.). Molecular function (MF), Biological processes (BP) and Cellular component (CC) (DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patel, S., Pachhigar, K., Ganvit, R. et al. Exploring Flowering Genes in Isabgol (Plantago ovata Forsk.) Through Transcriptome Analysis. Plant Mol Biol Rep 39, 192–211 (2021). https://doi.org/10.1007/s11105-020-01237-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01237-8

Keywords

Navigation