Abstract
Phytochromes (PHYs) have long been associated with classic photomorphogenic responses and recently implied with the regulation of plant productivity. We aimed to characterize these links in an important agronomic crop such as tomato (cv. Moneymaker) by evaluating biomass partitioning and morphophysiological parameters related to productivity under distinct light conditions in phyA, phyB1 and phyB2 tomato mutants. Under sun, PHY mutants presented lower leaf biomass during the vegetative phase the same way as the wild type (WT) under shading treatment. However, no difference regarding fruit biomass ratio (harvest index) was registered between WT and PHY mutants. phyA was the shortest genotype with lesser lateral branches and smaller xylem vessels and alongside phyB1, presented lesser leaf area. Net photosynthesis rate and photosystem II maximum potential quantum efficiency were not affected by phytochrome loss under sun condition. Nevertheless, PHY mutants showed lesser chlorophyll a content and stomata conductance and transpiration rates. Together, our data reveal that despite some morphophysiological and developmental impairments and the differences in biomass accumulation associated with the distinct PHYs under distinct light conditions, the plant harvest index is not affected by individual PHY losses under sun condition.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel-Mawgoud AMR, El-Abd SO, Singer SM, Abou-Hadid AF, Hsiao TC (1996) Effect of shade on the growth and yield of tomato plants. Acta Hortic 434:313–320. https://doi.org/10.17660/ActaHortic.1996.434.38
Alba R, Kelmenson PM, Cordonnier-Pratt M-M, Pratt LH (2000) The phytochrome gene family in tomato and the rapid differential evolution of this family in angiosperms. Mol Biol Evol 17:362–373. https://doi.org/10.1093/oxfordjournals.molbev.a026316
Alves FRR, Melo HC, Crispim-Filho AJ, Costa AC, Nascimento KJT, Carvalho RF (2016) Physiological and biochemical responses of photomorphogenic tomato mutants (cv. Micro-Tom) under water withholding. Acta Physiol Plant 38:155. https://doi.org/10.1007/s11738-016-2169-8
Arsovski AA, Zemke JE, Haagen BD, Kim S-H, Nemhauser JL (2018) Phytochrome B regulates resource allocation in Brassica rapa. J Exp Bot 69:2837–2846. https://doi.org/10.1093/jxb/ery080
Auge GA, Rugnone ML, Cortés LE, González CV, Zarlavsky G, Boccalandro HE, Sánchez RA (2012) Phytochrome A increases tolerance to high evaporative demand. Physiol Plant 146:228–235. https://doi.org/10.1111/j.1399-3054.2012.01625.x
Bianchetti RE, Cruz AB, Oliveira BS, Demarco D, Purgatto E, Peres LEP, Rossi M, Freschi L (2017) Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits. Sci Rep 7:7822. https://doi.org/10.1038/s41598-017-08448-2
Boccalandro HE, Ploschuk EL, Yanovsky MJ, Sánchez RA, Gatz C, Casal JJ (2003) Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol 133:1539–1546. https://doi.org/10.1104/pp.103.029579
Boccalandro HE, Rugnone ML, Moreno JE, Ploschuk EL, Serna L, Yanovsky MJ, Casal JJ (2009) Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. Plant Physiol 150:1083–1092. https://doi.org/10.1104/pp.109.135509
Brouwer B, Gardeström P, Keech O (2014) In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis. J Exp Bot 65:4037–4049
Cagnola JI, Ploschuk E, Benech-Arnold T, Finlayson SA, Casal JJ (2012) Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato. Plant Physiol 160:1110–1119. https://doi.org/10.1104/pp.112.201921
Carlson KD, Bhogale S, Anderson D, Tomanek L, Madlung A (2019) Phytochrome A Regulates Carbon Flux in Dark Grown Tomato Seedlings. Front Plant Sci 10:152. https://doi.org/10.3389/fpls.2019.00152
Casson SA, Hetherington AM (2014) Phytochrome B is required for light-mediated systemic control of stomatal development. Curr Biol 24:1216–1221. https://doi.org/10.1016/j.cub.2014.03.074
Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521. https://doi.org/10.1016/j.tplants.2007.10.001
Chen M, Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21:664–671. https://doi.org/10.1016/j.tcb.2011.07.002
Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Gen 38:87–117. https://doi.org/10.1146/annurev.genet.38.072902.092259
Costa GC, Marenco RA (2007) Fotossíntese, condutância estomática e potencial hídrico foliar em árvores jovens de andiroba (Carapa guianensis). Acta Amaz 37:229–234. https://doi.org/10.1590/S0044-59672007000200008
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Foreman J, Johansson H, Hornitschek P, Josse E-M, Fankhauser C, Halliday KJ (2011) Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J 65:441–452. https://doi.org/10.1111/j.1365-313X.2010.04434.x
Franklin KA, Praekelt U, Stoddart WM, Billingham OE, Halliday KJ, Whitelam GC (2003) Phytochromes B, D and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol 131:1340–1346. https://doi.org/10.1104/pp.102.015487
Gifford RM, Thorne JH, Hitz WD, Giaquinta RT (1984) Crop productivity and photoassimilate partitioning. Science 225:801–808. https://doi.org/10.1126/science.225.4664.801
Han Y-J, Song P-S, Kim J-I (2007) Phytochrome-mediated photomorphogenesis in plants. J Plant Biol 50:230–240. https://doi.org/10.1007/BF03030650
Hauser BA, Pratt LH, Cordonnier-Pratt M-M (1997) Absolute quantification of five phytochrome transcripts in seedlings and mature plants of tomato (Solanum lycopersicum L.). Planta 201:379–387. https://doi.org/10.1007/s004250050080
Husaineid SSH, Kok RA, Schreuder MEL, Hanumappa M, Cordonnier-Pratt M-M, Pratt LH, Van Der Plas LHW, Van Der Krol AR (2007) Overexpression of homologous phytochrome genes in tomato: exploring the limits of photoperception. J Exp Bot 58:615–626. https://doi.org/10.1093/jxb/erl253
Igamberdiev AU, Eprintsev AT, Fedorin DN, Popov VN (2014) Phytochrome-mediated regulation of plant respiration and photorespiration. Plant, Cell Environ 37:290–299. https://doi.org/10.1111/pce.12155
Kalaitzoglou P, Van Ieperen W, Harbinson J, Van der Meer M, Martinakos S, Weerheim K, Nicole CCS, Marcelis LFM (2019) Effects of continuous or end-of-day far-red light on tomato plant growth, morphology, light absorption, and fruit production. Front Plant Sci 10:322. https://doi.org/10.3389/fpls.2019.00322
Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. https://doi.org/10.1016/S0070-2153(10)91002-8
Kharshiing E, Sinha SP (2016) Deficiency in phytochrome A alters photosynthetic activity, leaf starch metabolism and shoot biomass production in tomato. J Photochem Photobiol B: Biol 165:157–162. https://doi.org/10.1016/j.jphotobiol.2016.10.026
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570. https://doi.org/10.1104/pp.114.237107
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Markesteijn L, Poorter L, Bongers F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am J Bot 94:515–525. https://doi.org/10.3732/ajb.94.4.515
Melo HC, Constantino EJ, Cacho RC, Carvalho RF (2014) Photosynthate partitioning and morphoanatomical aspects of photomorphogenic mutants of tomato. Biosci J 30: 447-457. http://www.seer.ufu.br/index.php/biosciencejournal/article/view/18031
Nishimura K, Ogawa T, Ashida H, Yokota A (2008) Molecular mechanisms of RuBisCO biosynthesis in higher plants. Plant Biotechnol 25:285–290. https://doi.org/10.5511/plantbiotechnology.25.285
Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Pratt LH, Cordonnier-Pratt MM, Hauser B, Caboche M (1995) Tomato contains two differentially expressed genes encoding B-type phytochromes, neither of which can be considered an ortholog of Arabidopsis phytochrome B. Planta 197:203–206. https://doi.org/10.1007/BF00239958
Qu M, Zheng G, Hamdani S, Essemine J, Song Q, Wang H, Chu C, Sirault X, Zhu X-G (2017) Leaf photosynthetic parameters related to biomass accumulation in a global rice diversity survey. Plant Physiol 175:248–258. https://doi.org/10.1104/pp.17.00332
Sandri MA, Andriolo JL, Witter M, Ross TD (2003) Effect of shading on tomato plants grown under greenhouse. Hortic Bras 21:642–645. https://doi.org/10.1590/S0102-05362003000400013
Schittenhelm S, Menge-Hartmann U, Oldenburg E (2004) Photosynthesis, carbohydrate metabolism and yield of phytochrome-B-overexpressing potatoes under different light regimes. Crop Sci 44:131–143. https://doi.org/10.2135/cropsci2004.0131
Schrager-Lavelle A, Herrera LA, Maloof JN (2016) Tomato phyE Is Required for Shade Avoidance in the Absence of phyB1 and phyB2. Front Plant Sci 7:1275. https://doi.org/10.3389/fpls.2016.01275
Sharrock RA (2008) The phytochrome red/far-red photoreceptor superfamily. Genome Biol 9:230. https://doi.org/10.1186/gb-2008-9-8-230
Shinomura T, Uchida K, Furuya M (2000) Elementary process of photoperception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiol 122:147–156. https://doi.org/10.1104/pp.122.1.147
Strasser B, Sánchez-Lamas M, Yanovsky MJ, Casal JJ, Cerdán PD (2010) Arabidopsis thaliana life without phytochromes. Proc Natl Acad Sci USA 107:4776–4781. https://doi.org/10.1073/pnas.0910446107
Tenhunen JD, Lange OL, Gebel J, Beyschlag W, Weber JA (1984) Changes in photosynthetic capacity, carboxylation efficiency and CO2 compensation point associated with midday stomatal closure and midday depression of net CO2 exchange of leaves of Quercus suber. Planta 162:193–203. https://doi.org/10.1007/BF00397440
Ulqodry TZ, Matsumoto F, Okimoto Y, Nose A, Zheng SH (2014) Study on photosynthetic responses and chlorophyll fluorescence in Rhizophora mucronata seedlings under shade regimes. Acta Physiol Plant 36:1903. https://doi.org/10.1007/s11738-014-1566-0
Wang H, Wang H (2015) Phytochrome signaling: time to lighten up the loose ends. Mol Plant 8:540–551. https://doi.org/10.1016/j.molp.2014.11.021
Weller JL, Schreuder ME, Smith H, Koornnef M, Kendrick RE (2000) Physiological interactions of phytochromes A, B1 and B2 in the control of development in tomato. Plant Journal 24:345–356. https://doi.org/10.1046/j.1365-313x.2000.00879.x
Yang D, Seaton DD, Krahmer J, Halliday KJ (2016) Photoreceptor effects on plant biomass, resource allocation, and metabolic state. Proc Natl Acad Sci USA 113:7667–7672. https://doi.org/10.1073/pnas.160130911
Zhang L, Copini P, Weemstra M, Sterck F (2016) Functional ratios among leaf, xylem and phloem areas in branches change with shade tolerance, but not with local light conditions, across temperate tree species. New Phytol 209:1566–1575. https://doi.org/10.1111/nph.13731
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mereb, E.L., Alves, F.R.R., Rezende, M.H. et al. Morphophysiological responses of tomato phytochrome mutants under sun and shade conditions. Braz. J. Bot 43, 45–54 (2020). https://doi.org/10.1007/s40415-020-00584-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-020-00584-w