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Increased gibberellin levels enhance light capture efficiency in tobacco plants and promote dry matter accumulation

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Abstract

Plants are constantly subjected to light variations in the environment, and plant hormones are one of the intermediaries between environmental signals and physiological responses. Among these responses, gibberellins (GAs) promote physiological changes that regulate plant growth and development patterns. Morphological changes, such as internode length and light absorbance maximization, are likely to induce plant performance increases leading to biomass accumulation. In this context, the hypothesis tested herein was that manipulation of GA levels can influence plant biomass accumulation by modifying the internode length and, consequently, light capture efficiency, with direct effects on plant biomass accumulation rates evaluated by unit leaf rate and growth analysis. For this, tobacco plants were cultivated in high- and low- irradiance environments under different gibberellic acid (GA3) and paclobutrazol (PAC, a GA biosynthesis inhibitor) concentrations as a tool to manipulate the internode length and plant height. Dry matter accumulation was evaluated in response to light capture efficiency and interception, energy content and anatomical stem changes. The results obtained and supported by a principal component analysis indicate that GAs are capable of promoting phenotypic changes in plants grown in both high and low irradiance environments, and that they trigger responses related with biomass accumulation by maximizing light capture performance in response to internode length in tobacco plants. The data presented herein emphasize that GAs are essential in promoting growth and biomass accumulation, especially in low irradiance environments.

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References

  • Alabadí D, Gallego-Bartolomé J, Orlando L et al (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53:324–335

    Article  PubMed  CAS  Google Scholar 

  • Amato R, Ramalho D, Monteiro C et al (2016) Scientia Horticulturae Water restriction, girdling and paclobutrazol on flowering and production of olive cultivars. Sci Hortic (Amsterdam) 200:197–204

    Article  CAS  Google Scholar 

  • Antunes WC, Daloso DM, Pinheiro DP et al (2017) Guard cell-specific down-regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environ Exp Bot 135:73–85

    Article  CAS  Google Scholar 

  • Baninasab B, Ghobadi C (2011) Influence of paclobutrazol and application methods on high-temperature stress injury in cucumber seedlings. J Plant Growth Regul 30:213–219

    Article  CAS  Google Scholar 

  • Bhattacharya A, Kourmpetli S, Davey MR (2010) Practical applications of manipulating plant architecture by regulating gibberellin metabolism. J Plant Growth Regul 29:249–256

    Article  CAS  Google Scholar 

  • 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 135:254–265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cipollini DF, Schultz JC (1999) Exploring cost constraints on stem elongation in plants using phenotypic manipulation. Am Nat 153:236–242

    Article  PubMed  Google Scholar 

  • Croce R, Van Amerongen H (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10:492–501

    Article  PubMed  CAS  Google Scholar 

  • Davies PJ (2010) Gibberellin biosynthesis and inactivation, 3rd edn. Springer, New York

    Google Scholar 

  • Dayan J, Schwarzkopf M, Avni A, Aloni R (2010) Enhancing plant growth and fiber production by silencing GA2-oxidase. Plant Biotechnol J 8:425–435

    Article  PubMed  CAS  Google Scholar 

  • Dayan J, Voronin N, Gong F et al (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. Plant Cell 24:66–79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Wit M, Galvão VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:513–537

    Article  PubMed  CAS  Google Scholar 

  • Delagrange S, Messier C, Lechowicz MJ, Dizengremel P (2004) Physiological, morphological and allocational plasticity in understory deciduous trees: importance of plant size and light availability. Tree Physiol 24:775–784

    Article  PubMed  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Cost and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  PubMed  CAS  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  PubMed  CAS  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationship in leaves of C3 plants. Oecologia 78:9–19

    Article  PubMed  Google Scholar 

  • Falcioni R, Moriwaki T, Bonato CM et al (2017) Distinct growth light and gibberellin regimes alter leaf anatomy and reveal their influence on leaf optical properties. Environ Exp Bot 140:86–95

    Article  CAS  Google Scholar 

  • Ford ED (2014) The dynamic relationship between plant architecture and competition. Front Plant Sci 5:275

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukuda N, Ajima C, Yukawa T, Olsen JE (2016) Antagonistic action of blue and red light on shoot elongation in petunia depends on gibberellin, but the effects on flowering are not generally linked to gibberellin. Environ Exp Bot 121:102–111

    Article  CAS  Google Scholar 

  • Galvão VC, Fankhauser C (2015) Sensing the light environment in plants: photoreceptors and early signaling steps. Curr Opin Neurobiol 34:46–53

    Article  PubMed  CAS  Google Scholar 

  • Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92

    Article  Google Scholar 

  • Guo H, Wang Y, Liu H et al (2015) Exogenous GA3 application enhances xylem development and induces the expression of secondary wall biosynthesis related genes in Betula platyphylla. Int J Mol Sci 16:22960–22975

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hedden P, Sponsel V (2015) A century of gibberellin research. J Plant Growth Regul 34:740–760

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hedden P, Thomas SG (2016) Annual plant review: the gibberellins, 1st edn. Wiley, New York

    Book  Google Scholar 

  • Hirose T (2005) Development of the Monsi-Saeki theory on canopy structure and function. Ann Bot 95:483–494

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90:37–42

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibrahim L (2001) An investigation of wound healing in sugar beet roots using light and fluorescence microscopy. Ann Bot 88:313–320

    Article  Google Scholar 

  • Ishida H, Izumi M, Wada S, Makino A (2014) Roles of autophagy in chloroplast recycling. Biochim Biophys Acta 1837:512–521

    Article  PubMed  CAS  Google Scholar 

  • Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A

    Google Scholar 

  • Kurepin LV, Pharis RP (2014) Light signaling and the phytohormonal regulation of shoot growth. Plant Sci 229:280–289

    Article  PubMed  CAS  Google Scholar 

  • Kurepin LV, Pharis RP, Reid DM, Chinnappa CC (2006) Involvement of gibberellins in the stem elongation of sun and shade ecotypes of Stellaria longipes that is induced by low light irradiance. Plant, Cell Environ 29:1319–1328

    Article  CAS  Google Scholar 

  • Kurepin LV, Emery RJN, Pharis RP, Reid DM (2007) The interaction of light quality and irradiance with gibberellins, cytokinins and auxin in regulating growth of Helianthus annuus hypocotyls. Plant, Cell Environ 30:147–155

    Article  CAS  Google Scholar 

  • Lambers H, Poorter H (2004) Inherent variation in growth rate between higher plants: a search for physiological causes and ecology consequences. Adv Ecol Res 34:283–362

    Article  Google Scholar 

  • Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13:571–577

    Article  PubMed  CAS  Google Scholar 

  • Nagel OW, Lambers H (2002) Changes in the acquisition and partitioning of carbon and nitrogen in the gibberellin-deficient mutants A70 and W335 of tomato (Solanum lycopersicum L.). Plant, Cell Environ 25:883–891

    Article  CAS  Google Scholar 

  • Nagel OW, Konings H, Lambers H (2001) Growth rate and biomass partitioning of wildtype and low-gibberellin tomato (Solanum lycopersicum) plants growing at a high and low. Physiol Plant 111:33–39

    Article  CAS  Google Scholar 

  • Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30:1052–1071

    Article  PubMed  CAS  Google Scholar 

  • Pearcy RW (2007) Responses of plants to heterogeneous light environments. In: Pugnaire F, Valladares F (eds) Functional plant ecology, 2nd edn. CRC Press, New York, pp 213–258

    Google Scholar 

  • Pearcy RW, Muraoka H, Valladares F (2005) Crown architecture in sun and shade environments: assessing function and trade-offs with a three-dimensional simulation model. New Phytol 166:791–800

    Article  PubMed  Google Scholar 

  • Poorter H (1994) Construction costs and payback time of biomass: a whole plant perspective. In: Roy J, Garnier E (eds) A whole plant perspective on carbon-nitrogen interactions, 1st edn. SPB Academic Publishing, Amsterdam, pp 111–127

    Google Scholar 

  • Poorter H, Niklas KJ, Reich PB et al (2011) Biomass allocation to leaves, stems and roots: meta-analysis of interspecific variation and environmental control. New Phytol 193:30–50

    Article  PubMed  CAS  Google Scholar 

  • Pugnaire F, Valladares F (2007) Functional plant ecology, 2nd edn. CRC Press, New York

    Google Scholar 

  • Rademacher W (2015) Plant growth regulators: backgrounds and uses in plant production. J Plant Growth Regul 34:845–872

    Article  CAS  Google Scholar 

  • Ribeiro DM, Araújo WL, Fernie AR et al (2012) Translatome and metabolome effects triggered by gibberellins during rosette growth in Arabidopsis. J Exp Bot 63:2769–2786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roro AG, Dukker SAF, Melby TI et al (2017) UV-B-induced inhibition of stem elongation and leaf expansion in pea depends on modulation of gibberellin metabolism and intact gibberellin signalling. J Plant Growth Regul 36:680–690

    Article  CAS  Google Scholar 

  • Sarlikioti V, De Visser PHB, Buck-Sorlin GH, Marcelis LFM (2011) How plant architecture affects light absorption and photosynthesis in tomato: towards an ideotype for plant architecture using a functionalstructural plant model. Ann Bot 108:1065–1073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542

    Article  PubMed  CAS  Google Scholar 

  • Takenaka A (1994) Effects of leaf blade narrowness and petiole length on the light capture efficiency of a shoot. Ecol Res 9:109–114

    Article  Google Scholar 

  • Thetford M, Warren SL, Blazich FA, Thomas JF (1995) Response of Forsythia xintermedia spectabilis to uniconazole. 2. Leaf and stem anatomy, chlorophyll, and photosynthesis. J Am Soc Hortic Sci 120:983–988

    CAS  Google Scholar 

  • Tokunaga N, Uchimura N, Sato Y (2006) Involvement of gibberellin in tracheary element differentiation and lignification in Zinnia elegans xylogenic culture. Protoplasma 228:179–187

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson PB (1987) Architecture of tropical plants. Annu Rev Ecol Syst 18:1–21

    Article  Google Scholar 

  • Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257

    Article  Google Scholar 

  • Valladares F, Pugnaire F (1999) Tradeoffs between irradiance capture and avoidance in semi-arid environments assessed with a crown architecture model. Ann Bot 83:459–469

    Article  Google Scholar 

  • Vandenbussche F, Pierik R, Millenaar FF et al (2005) Reaching out of the shade. Curr Opin Plant Biol 8:462–468

    Article  PubMed  CAS  Google Scholar 

  • Vermeulen PJ, Stuefer JF, During HJ, Anten NPR (2008) Leaf investment and light partitioning among leaves of different genotypes of the clonal plant Potentilla reptans in a dense stand after 5 years of competition. Ann Bot 102:935–943

    Article  PubMed  PubMed Central  Google Scholar 

  • Wada M, Shimazaki K, Iino M (2005) Light sensing in plants, 1st edn. Springer, New York

    Book  Google Scholar 

  • Walters MB, Reich PB (2000) Seed size, nitrogen supply, and growth rate affect tree seedling survival in deep shade. Ecology 81:1887–1901

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Education, Upper Saddle River

    Google Scholar 

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Acknowledgements

This study was partially funded by the Brazilian National Council for Technological and Scientific Development–CNPq, Brazil (Universal—443102/2014-7). Scholarships granted by the Brazilian Government (R.F. and T.M.—CAPES,) are gratefully acknowledged. The authors thanks to COMCAP (CMI)—UEM for the microscopy fluorescence use and anonymous reviewers for significantly contributions to our manuscript.

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Authors and Affiliations

  1. Laboratório de Ecofisiologia Vegetal, Departamento de Biologia, Universidade Estadual de Maringá (UEM), Av. Colombo 5790, Jd. Universitário, Maringá, Paraná, 87020-900, Brazil

    Renan Falcioni, Thaise Moriwaki, Carlos Moacir Bonato & Werner Camargos Antunes

  2. Laboratório de Ecologia Energética, Núcleo de Pesquisa em Limnologia, Universidade Estadual de Maringá (UEM), Av. Colombo 5790, Jd. Universitário, Maringá, Paraná, 87020-900, Brazil

    Evanilde Benedito

  3. Laboratório de Histotécnica Vegetal, Universidade Estadual de Maringá (UEM), Av. Colombo 5790, Jd. Universitário, Maringá, Paraná, 87020-900, Brazil

    Luiz Antônio de Souza

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  1. Renan Falcioni
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  2. Thaise Moriwaki
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Correspondence to Werner Camargos Antunes.

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Falcioni, R., Moriwaki, T., Benedito, E. et al. Increased gibberellin levels enhance light capture efficiency in tobacco plants and promote dry matter accumulation. Theor. Exp. Plant Physiol. 30, 235–250 (2018). https://doi.org/10.1007/s40626-018-0118-1

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