Abstract
Main conclusion
Blue light exposure delays tomato seed germination by decreasing endosperm-degrading hydrolase activities, a process regulated by CRY1a-dependent signaling and the hormonal balance between ABA and GA.
Abstract
The germination of tomato seeds (Solanum lycopersicum L.) is tightly controlled by an internal hormonal balance, which is also influenced by environmental factors such as light. In this study, we investigated the blue light (BL)-mediated impacts on physiological, biochemical, and molecular processes during the germination of the blue light photoreceptor CRYPTOCHROME 1a loss-of-function mutant (cry1a) and of the hormonal tomato mutants notabilis (not, deficient in ABA) and procera (pro, displaying a GA-constitutive response). Seeds were germinated in a controlled chamber in the dark and under different intensities of continuous BL (ranging from 1 to 25 µmol m−2 s−1). In general, exposure to BL delayed tomato seed germination in a fluency rate-dependent way due to negative impacts on the activities of endosperm-degrading hydrolases, such as endo-β-mannanase, β-mannosidase, and α-galactosidase. However, not and pro mutants presented higher germination speed index (GSI) compared to WT despite the BL influence, associated with higher hydrolase activities, especially evident in pro, indicating that the ABA/GA hormonal balance is important to diminish BL inhibition over tomato germination. The cry1a germination percentage was higher than in WT in the dark but its GSI was lower under BL exposure, suggesting that functional CRY1a is required for BL-dependent germination. BL inhibits the expression of GA-biosynthetic genes, and induces GA-deactivating and ABA-biosynthetic genes. The magnitude of the BL influence over the hormone-related transcriptional profile is also dependent upon CRY1a, highlighting the complex interplay between light and hormonal pathways. These results contribute to a better understanding of BL-induced events behind the photoregulation of tomato seed germination.
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Data availability
The experimental datasets are available upon reasonable request to the corresponding author.
Abbreviations
- BL:
-
Blue light
- CRY:
-
Cryptochrome
- G%:
-
Germination percentage
- GSI:
-
Germination speed index
- T50:
-
Time to reach 50% total germination
References
Appenroth KJ, Lenk G, Goldau L, Sharma R (2006) Tomato seed germination: regulation of different response modes by phytochrome B2 and phytochrome A. Plant Cell Environ 29:701–709. https://doi.org/10.1111/j.1365-3040.2005.01455.x
Arana MV, Burgin MJ, De Miguel LC, Sánchez RA (2007) The very-low-fluence and high-irradiance responses of the phytochromes have antagonistic effects on germination, mannan-degrading activities, and DfGA3ox transcript levels in Datura ferox seeds. J Exp Bot 58:3997–4004. https://doi.org/10.1093/jxb/erm256
Arunraj R, Skori L, Kumar A, Hickerson NMN, Shoma N, Vairamani M, Samuel MA (2020) Spatial regulation of alpha-galactosidase activity and its influence on raffinose family oligosaccharides during seed maturation and germination in Cicer arietinum. Plant Signal Behav 15(8):1709707. https://doi.org/10.1080/15592324.2019.1709707
Auge GA, Perelman S, Crocco CD, Sánchez RA, Botto JF (2009) Gene expression analysis of light-modulated germination in tomato seeds. New Phytol 183(2):301–314. https://doi.org/10.1111/j.1469-8137.2009.02867.x
Balarynová J, Danihlík J, Fellner M (2018) Changes in plasma membrane aquaporin gene expression under osmotic stress and blue light in tomato. Acta Physiol Plant 40:27. https://doi.org/10.1007/s11738-017-2602-7
Barrero JM, Jacobsen JV, Talbot MJ, White RG, Swain SM, Garvin DF, Gubler F (2012) Grain dormancy and light quality effects on germination in the model grass Brachypodium distachyon. New Phytol 193(2):376–386. https://doi.org/10.1111/j.1469-8137.2011.03938.x
Barrero JM, Downie AB, Xu Q, Gubler F (2014) A role for barley CRYPTOCHROME1 in light regulation of grain dormancy and germination. Plant Cell 26(3):1094–1104. https://doi.org/10.1105/tpc.113.121830
Bassel GW, Mullen RT, Bewley JD (2008) procera is a putative DELLA mutant in tomato (Solanum lycopersicum): Effects on the seed and vegetative plant. J Exp Bot 59(3):585–593. https://doi.org/10.1093/jxb/erm354
Bewley JD, Banik M, Bourgault R, Feurtado JA, Toorop P, Hilhorst HW (2000) Endo-β-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening. J Exp Bot 51(344):529–538. https://doi.org/10.1093/jexbot/51.344.529
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17(4):427–431. https://doi.org/10.1046/j.1365-313X.1999.00386.x
Carrera E, Ruiz-Rivero O, Peres LEP, Atares A, Garcia-Martinez JL (2012) Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol 160(3):1581–1596. https://doi.org/10.1104/pp.112.204552
Carvalho RF, Campos ML, Pino LE et al (2011) Convergence of developmental mutants into a single tomato model system:’Micro-Tom’as an effective toolkit for plant development research. Plant Methods 7(1):18. https://doi.org/10.1186/1746-4811-7-18
Chen S, Wang X, Zhang L et al (2016) Identification and characterization of tomato gibberellin 2-oxidases (GA2oxs) and effects of fruit-specific SlGA2ox1 overexpression on fruit and seed growth and development. Hortic Res 3:16059. https://doi.org/10.1038/hortres.2016.59
Cruz AB, Bianchetti RE, Alves FRR, Purgatto E, Peres LEP, Rossi M, Freschi L (2018) Light, ethylene and auxin signaling interaction regulates carotenoid biosynthesis during tomato fruit ripening. Front Plant Sci 9:1370. https://doi.org/10.3389/fpls.2018.01370
D’Amico-Damião V, Santos JC, Girotto NC, Carvalho RF (2019) Cryptochrome 1a influences source-sink partitioning during different stages of growth in tomato. Theor Ex Plant Physiol 31(2):295–302. https://doi.org/10.1007/s40626-019-00141-1
D’Amico-Damião V, Lúcio JCB, Oliveira R, Gaion LA, Barreto RF, Carvalho RF (2021) Cryptochrome 1a depends on blue light fluence rate to mediate osmotic stress responses in tomato. J Plant Physiol 258:153374. https://doi.org/10.1016/j.jplph.2021.153374
Downie B, Gurusinghe S, Dahal P et al (2003) Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131(3):1347–1359. https://doi.org/10.1104/pp.016386
Eckstein A, Jagiełło-Flasińska D, Lewandowska A, Hermanowicz P, Appenroth KJ, Gabryś H (2016) Mobilization of storage materials during light-induced germination of tomato (Solanum lycopersicum) seeds. Plant Physiol Biochem 105:271–281. https://doi.org/10.1016/j.plaphy.2016.05.008
Evenari M, Neumann G, Stein G (1957) Action of blue light on the germination of seeds. Nature 180:609–610. https://doi.org/10.1038/180609b0
Facella P, Lopez L, Chiappetta A, Bitonti MB, Giuliano G, Perrotta G (2006) CRY-DASH gene expression is under the control of the circadian clock machinery in tomato. FEBS Lett 580(19):4618–4624. https://doi.org/10.1016/j.febslet.2006.07.044
Fantini E, Sulli M, Zhang L et al (2019) Pivotal roles of cryptochromes 1a and 2 in tomato development and physiology. Plant Physiol 179(2):732–748. https://doi.org/10.1104/pp.18.00793
Gavassi MA, Fernandes GC, Monteiro CC, Peres LEP, Carvalho RF (2014) Seed germination in tomato: a focus on interaction between phytochromes and gibberellins or abscisic acid. Am J Plant Sci 5:2163–2169. https://doi.org/10.4236/ajps.2014.514229
Hoang HH, Sechet J, Bailly C, Leymarie J, Corbineau F (2014) Inhibition of germination of dormant barley (Hordeum vulgare L.) grains by blue light as related to oxygen and hormonal regulation. Plant Cell Environ 37(6):1393–1403. https://doi.org/10.1111/pce.12239
Hofmann N (2014) Cryptochromes and seed dormancy: the molecular mechanism of blue light inhibition of grain germination. Plant Cell 26(3):846. https://doi.org/10.1105/tpc.114.124727
Izzo LG, Mele BH, Vitale L, Vitale E, Arena C (2020) The role of monochromatic red and blue light in tomato early photomorphogenesis and photosynthetic traits. Environ Exp Bot 179:104195. https://doi.org/10.1016/j.envexpbot.2020.104195
Kubala S, Wojtyla Ł, Quinet M, Lechowska K, Lutts S, Garnczarska M (2015) Enhanced expression of the proline synthesis gene P5CSA in relation to seed osmopriming improvement of Brassica napus germination under salinity stress. J Plant Phys 183:1–12. https://doi.org/10.1016/j.jplph.2015.04.009
Lara-Núñez A, Sánchez-Nieto S, Luisa Anaya A, Cruz-Ortega R (2009) Phytotoxic effects of Sicyos deppei (Cucurbitaceae) in germinating tomato seeds. Physiol Plant 136(2):180–192. https://doi.org/10.1111/j.1399-3054.2009.01228.x
Lariguet P, Ranocha P, De Meyer M, Barbier O, Penel C, Dunand C (2013) Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta 238(2):381–395. https://doi.org/10.1007/s00425-013-1901-5
Lee KP, Piskurewicz U, Turečková V et al (2012) Spatially and genetically distinct control of seed germination by phytochromes A and B. Genes Dev 26(17):1984–1996. https://doi.org/10.1101/gad.194266.112
Liu CC, Ahammed GJ, Wang GT, Xu CJ, Chen KS, Zhou YH, Yu JQ (2018) Tomato CRY1a plays a critical role in the regulation of phytohormone homeostasis, plant development, and carotenoid metabolism in fruits. Plant Cell Environ 41(2):354–366. https://doi.org/10.1111/pce.13092
Livne S, Lor VS, Nir I et al (2015) Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 27(6):1579–1594. https://doi.org/10.1105/tpc.114.132795
Mérai Z, Graeber K, Wilhelmsson P et al (2019) Aethionema arabicum: a novel model plant to study the light control of seed germination. J Exp Bot 70(12):3313–3328. https://doi.org/10.1093/jxb/erz146
Mo B, Bewley DJ (2002) β-Mannosidase (EC 3.2 1.25) activity during and following germination of tomato (Lycopersicon esculentum Mill.) seeds. Purification, cloning and characterization. Planta 215(1):141–152. https://doi.org/10.1007/s00425-001-0725-x
Mo B, Bewley JD (2003) The relationship between β-mannosidase and endo-β-mannanase activities in tomato seeds during and following germination: a comparison of seed populations and individual seeds. J Exp Bot 54:2503–2510. https://doi.org/10.1093/jxb/erg274
Moles TM, Guglielminetti L, Reyes TH (2019) Differential effects of sodium chloride on germination and post-germination stages of two tomato genotypes. Sci Hortic 257:108730. https://doi.org/10.1016/j.scienta.2019.108730
Moreira LRS, Filho EXF (2008) An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotech 79:165–178. https://doi.org/10.1007/s00253-008-1423-4
Nakaune M, Hanada A, Yin YG, Matsukura C, Yamaguchi S, Ezura H (2012) Molecular and physiological dissection of enhanced seed germination using short-term low-concentration salt seed priming in tomato. Plant Physiol Biochem 52:28–37. https://doi.org/10.1016/j.plaphy.2011.11.005
Ninu L, Ahmad M, Miarelli C, Cashmore AR, Giuliano G (1999) Cryptochrome 1 controls tomato development in response to blue light. Plant J 18(5):551–556. https://doi.org/10.1046/j.1365-313X.1999.00466.x
Nomaguchi M, Nonogaki H, Morohashi Y (1995) Development of galactomannan-hydrolyzing activity in the micropylar endosperm tip of tomato seed prior to germination. Physiol Plant 94(1):105–109. https://doi.org/10.1111/j.1399-3054.1995.tb00790.x
Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiol 123(4):1235–1246. https://doi.org/10.1104/pp.123.4.1235
Perrotta G, Yahoubyan G, Nebuloso E, Renzi L, Giuliano G (2001) Tomato and barley contain duplicated copies of cryptochrome 1. Plant Cell Environ 24(9):991–998. https://doi.org/10.1046/j.0016-8025.2001.00736.x
Piterková J, Luhová L, Hofman J, Turečková V, Novák O, Petřivalský M, Fellner M (2012) Nitric oxide is involved in light-specific responses of tomato during germination under normal and osmotic stress conditions. Ann Bot 110(4):767–776. https://doi.org/10.1093/aob/mcs141
R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Van Raij B, Cantarella H, Quaggio JA, Furlani MC (1997) Recomendações de abudação e calagem para o estado de São Paulo, Boletim Técnico 100, 2nd edn. IAC, Campinas.
Ravindran P, Verma V, Stamm P, Kumar PP (2017) A novel RGL2–DOF6 complex contributes to primary seed dormancy in Arabidopsis thaliana by regulating a GATA transcription factor. Mol Plant 10(10):1307–1320. https://doi.org/10.1016/j.molp.2017.09.004
Reid JSG, Meier H (1973) Enzymic activities and galactomannan mobilisation in germinating seeds of fenugreek (Trigonella foenum-graecum L. Leguminosae). Planta 112(4):301–308
Sánchez RA, De Miguel L (1997) Phytochrome promotion of mannan-degrading enzyme activities in the micropylar endosperm of Datura ferox seeds requires the presence of the embryo and gibberellin synthesis. Seed Sci Res 7(1):27–34. https://doi.org/10.1017/S0960258500003330
Seo M, Hanada A, Kuwahara A et al (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48(3):354–366. https://doi.org/10.1111/j.1365-313X.2006.02881.x
Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69(4):463. https://doi.org/10.1007/s11103-008-9429-y
Shu K, Liu X, Xie Q, He Z (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45. https://doi.org/10.1016/j.molp.2015.08.010
Stawska M, Oracz K (2019) phyB and HY5 are involved in the blue light-mediated alleviation of dormancy of Arabidopsis seeds possibly via the modulation of expression of genes related to light, GA, and ABA. Int J Mol Sci 20(23):5882. https://doi.org/10.3390/ijms20235882
Still DW, Bradford KJ (1997) Endo-β-mannanase activity from individual tomato endosperm caps and radicle tips in relation to germination rates. Plant Physiol 113(1):21–29. https://doi.org/10.1104/pp.113.1.21
Weller JL, Perrotta G, Schreuder ME, Van Tuinen A, Koornneef M, Giuliano G, Kendrick RE (2001) Genetic dissection of blue-light sensing in tomato using mutants deficient in cryptochrome 1 and phytochromes A, B1 and B2. Plant J 25(4):427–440. https://doi.org/10.1046/j.1365-313x.2001.00978.x
Xu P, Xiang Y, Zhu H et al (2009) Wheat cryptochromes: subcellular localization and involvement in photomorphogenesis and osmotic stress responses. Plant Physiol 149(2):760–774. https://doi.org/10.1104/pp.108.132217
Yang R, Chu Z, Zhang H et al (2015) The mechanism underlying fast germination of tomato cultivar LA2711. Plant Sci 238:241–250. https://doi.org/10.1016/j.plantsci.2015.06.012
Yang L, Liu S, Lin R (2020) The role of light in regulating seed dormancy and germination. J Int Plant Biol 62:1310–1326. https://doi.org/10.1111/jipb.13001
Acknowledgements
Ph.D. fellowship granted to Reginaldo de Oliveira was financed by the Coordination for the Improvement of Higher Education Personnel–Brazil (CAPES) (Finance Code 001) and the financial support was obtained through São Paulo Research Foundation (FAPESP) (grant number 2018/20748-3).
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RO and RFC conceived and designed the experiments. RO conducted the experiments and analyses. ERP, LDLG and LF provided experimental assistance. RO and FRRA analyzed the data. RO wrote the first draft of the manuscript. FRRA, LAG, and RFC revised the manuscript. RFC is the corresponding author. All authors read and approved the final manuscript.
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de Oliveira, R., Alves, F.R.R., da Rocha Prado, E. et al. CRYPTOCHROME 1a-mediated blue light perception regulates tomato seed germination via changes in hormonal balance and endosperm-degrading hydrolase dynamics. Planta 257, 67 (2023). https://doi.org/10.1007/s00425-023-04100-8
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DOI: https://doi.org/10.1007/s00425-023-04100-8