Transcriptional foliar profile of the C3-CAM bromeliad Guzmania monostachia


Autoři: Helenice Mercier aff001;  Maria Aurineide Rodrigues aff001;  Sónia Cristina da Silva Andrade aff002;  Luiz Lehmann Coutinho aff003;  Bruno Nobuya Katayama Gobara aff001;  Alejandra Matiz aff001;  Paulo Tamaso Mioto aff004;  Ana Zangirolame Gonçalves aff001
Působiště autorů: Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil aff001;  Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil aff002;  Departamento de Zootecnia, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, São Paulo, Brazil aff003;  Departamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Santa Catarina, Brazil aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224429

Souhrn

Guzmania monostachia is an epiphytic tank bromeliad that displays the inducible CAM photosynthesis under stressful conditions and had the highest stomata density in the leaf apex, while the base portion has the highest density of trichomes, which are specialized structures used to acquire water and nutrients from the tank solution. In order to correlate the genetic factors behind these morpho-physiological characteristics along the leaf blade of G. monostachia, a comparative transcriptome analysis was performed to identify the functional enriched pathways and unigenes that could play a role in the apical, middle and basal leaf portions. A total of 653 million reads were used for de novo transcriptome assembly, resulting in 48,051 annotated unigenes. Analysis of differentially expressed genes (DEGs) among distinct leaf regions revealed that 806 DEGs were upregulated in the apex compared to the middle portion, while 9685 DEGs were upregulated in the apex and 9784 DEGs were upregulated in the middle portions compared to the base. Our outcomes correlated some DEGs and identified unigenes with their physiological functions, mainly suggesting that the leaf apex was related to the regulation of stomatal movement, production of chlorophyll, cellular response to stress, and H2O2 catabolic process. In contrast, the middle portion showed DEGs associated with the transport of amino acids. Furthermore, DEGs from the leaf base were mainly correlated with responses to nutrients and nitrogen compounds, regulation of potassium ion import, response to water deprivation, and trichome branching, indicating that, at least in part, this leaf portion can replace some of the root functions of terrestrial plants. Therefore, possibly candidate unigenes and enriched pathways presented here could be prospected in future experimental work, opening new possibilities to bioengineer non-inducible CAM plants and/or improve the fertilization use efficiency by increasing leaf nutrient acquisition of crop plants.

Klíčová slova:

Cellular stress responses – Gene expression – Gene ontologies – Chlorophyll – Leaves – Sequence assembly tools – Transcriptome analysis – Trichomes


Zdroje

1. Lüttge U. 2010. Ability of crassulacean acid metabolism plants to overcome interacting stresses in tropical environments. AoB Plants: plq005. doi: 10.1093/aobpla/plq005 22476063

2. Rodrigues MA, Freschi L, Pereira PN, Mercier H. 2014. Interactions between nutrients and crassulacean acid metabolism, in Progress in Botany, eds Lüttge U, Cánovas FM, Munch J, Pretzsch H, Risueno MC, Leuschner C(Berlin: Springer-Verlag), 167–186.

3. Pikart FC, Marabesi MA, Mioto PT, Gonçalves AZ, Matiz A, Alves FRR, Mercier H, Aidar MPM. 2018. The contribution of weak CAM to the photosynthetic metabolic activities of a bromeliad species under water deficit. Plant Physiology and Biochemistry 123: 297–303. doi: 10.1016/j.plaphy.2017.12.030 29278846

4. Takahashi CA, Mercier H. 2011. Nitrogen metabolism in leaves of a tank epiphytic bromeliad: characterization of a spatial and functional division. Journal of Plant Physiology 168: 1208–1216. doi: 10.1016/j.jplph.2011.01.008 21333380

5. Kleingesinds CK, Gobara BNK, Mancilha D, Rodrigues MA, Demarco D, Mercier H. 2018. Impact of tank formation on distribution and cellular organization of trichomes within Guzmania monostachia rosette. Flora 243: 11–18.

6. Abreu ME, Carvalho V, Mercier H. 2018. Antioxidant capacity along the leaf blade of the C3-CAM facultative bromeliad Guzmania monostachia under water deficit conditions. Functional Plant Biology 45: 620–629.

7. Pereira PN, Gaspar M, Smith JAC, Mercier H. 2018. Ammonium intensifies CAM photosynthesis and counteracts drought by increasing malate transport and antioxidant capacity in Guzmania monostachia. Journal of Experimental Botany 69: 1993–2003. doi: 10.1093/jxb/ery054 29462338

8. Ong WD, Voo LYC, Kumar VS. 2012. De novo assembly, characterization and functional annotation of pineapple fruit transcriptome through massively parallel sequencing. PLoS ONE 7:e46937. doi: 10.1371/journal.pone.0046937 23091603

9. Ma J, Kanakala S, He Y, Zhang J, Zhong X. 2015. Transcriptome sequence analysis of an ornamental plant, Ananas comosus var. bracteatus, revealed the potential unigenes involved in terpenoid and phenylpropanoid biosynthesis. PLoS ONE 10: e0119153. doi: 10.1371/journal.pone.0119153 25769053

10. Liu CH, Fan C. 2016. De novo transcriptome assembly of floral buds of pineapple and identification of differentially expressed genes in response to ethephon induction. Frontiers in Plant Sciences 7:203. doi: 10.3389/fpls.2016.00203 26955375

11. Li Z, Wang J, Zhang X, Lei M, Fu Y, Zhang J, Wang Z, Xu L. 2016. Transcriptome sequencing determined flowering pathway genes in Aechmea fasciata treated with ethylene. Journal of Plant Growth Regulation 35: 316–329.

12. Palma-Silva C, Ferro M, Bacci M, Turchetto-Zolet AC. 2016. De novo assembly and characterization of leaf and floral transcriptomes of the hybridizing bromeliad species (Pitcairnia spp.) adapted to Neotropical Inselbergs. Molecular Ecology Resources 16: 1012–1022. doi: 10.1111/1755-0998.12504 26849180

13. Mioto PT, Mercier H. 2013. Abscisic acid and nitric oxide signaling in two different portions of detached leaves of Guzmania monostachia with CAM up-regulated by drought. Journal of Plant Physiology 170: 996–1002. doi: 10.1016/j.jplph.2013.02.004 23523467

14. Pereira PN, Purgatto E, Mercier H. 2013. Spatial division of phosphoenolpyruvate carboxylase and nitrate reductase activity and its regulation by cytokinins in CAM-induced leaves of Guzmania monostachia (Bromeliaceae). Journal of Plant Physiology 170: 1067–1074. doi: 10.1016/j.jplph.2013.03.005 23591079

15. Rodrigues MA, Hamachi L, Mioto PT, Purgatto E, Mercier H. 2016. Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia. Plant Physiology and Biochemistry 108: 400–411. doi: 10.1016/j.plaphy.2016.08.010 27552178

16. Males J. 2017. Hydraulics link leaf shape and environmental niche in terrestrial bromeliads. Biotropica 49: 891–902.

17. Knudson L. 1946. A new nutrient solution for germination for orchid seed. American Orchid Society Bulletin 15: 214–217.

18. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15: 473–479.

19. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29: 644–652. doi: 10.1038/nbt.1883 21572440

20. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8: 1494–1512. doi: 10.1038/nprot.2013.084 23845962

21. Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659. doi: 10.1093/bioinformatics/btl158 16731699

22. Camacho C, Madden T, Ma N, Tao T, Agarwala R, Morgulis A. 2016. BLAST command line applications user manual. National Center for Biotechnology Information (US). Available at: http://www.ncbi.nlm.nih.gov/books/NBK1763/ [accessed 05 Jul 2016].

23. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474

24. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359. doi: 10.1038/nmeth.1923 22388286

25. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550. doi: 10.1186/s13059-014-0550-8 25516281

26. Gentleman R, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5: R80. doi: 10.1186/gb-2004-5-10-r80 15461798

27. Benzing DH. 2000. Bromeliaceae: profile of an adaptive radiation. Cambridge University Press.

28. Zotz G, Reichling P, Valladares F. 2002. A simulation study on the importance of size-related changes in leaf morphology and physiology for carbon gain in an epiphytic bromeliad. Annals of Botany 90: 437–443. doi: 10.1093/aob/mcf208 12324266

29. Evans D. E. 2004. Aerenchyma formation. New Phytologist 161: 35–49.

30. Kleingesinds CK, Gobara BNK, Mancilha D, Rodrigues MA, Demarco D, Mercier H. 2018. Impact of tank formation on distribution and cellular organization of trichomes within Guzmania monostachia rosette. Flora 243: 11–18.


Článek vyšel v časopise

PLOS One


2019 Číslo 10