Response of the photosynthetic apparatus to a flowering-inductive period by water stress in Citrus

The photosynthetic responses to a flowering-inductive water-stress period and recovery were studied and compared in two Citrus species. Under greenhouse conditions, Fino lemon and Owari satsuma trees were subjected to moderate (-2 MPa at predawn) and severe (-3 MPa) water stress levels and were re-watered after 60 days. Vegetative growth was inhibited during the stress assays, and strong defoliation levels were reported, especially in Fino lemon. In both species, bud sprouting was induced after re-watering. Flowers and vegetative shoots developed in Owari satsuma after a drought period, and the development was independent of the stress level. In Fino lemon, vegetative shoots and flowers were primarily formed after moderate and severe stress, respectively. The photosynthetic rate and stomatal conductance were reduced by water stress, and a marked increase in water-use efficiency at the moderate water deficit level was observed. Nevertheless, the photosynthetic apparatus was not damaged, since the maximum quantum yield, photosynthetic pigment concentrations and Rubisco level and activity did not change. Furthermore, the measured malonyldialdehyde (MDA) and peroxidase activity indicated that oxidative stress was not specifically triggered by water stress in our study. Therefore, the gas exchange, fluorescence and biochemical parameters suggested that diffusional limitations to photosynthesis predominated in both of the studied Citrus species, and explained the rapid recovery of the photosynthetic parameters after rehydration. The net CO 2 fixation rate and stomatal conductance were recovered within 24 h in Fino lemon, whereas 3 days were required in Owari satsuma. This suggests the presence of some metabolic limitations in the latter species. Furthermore, the sensibility of the defoliation rates, the accumulation of proline and the stomatal behaviour in response to water stress indicated a higher drought tolerance of Fino lemon, according to its better acclimation to hot climates. © 2011 Springer-Verlag.The authors thank Dr. J. Moreno and co-workers from the Departamento de Bioquimica of the Universidad de Valencia for his help and support in the Rubisco assays, and Dr. F. Fornes, Dr. A. Calatayud and Dr. E. Primo-Millo for the critical review of the manuscript. This work was funded by the Universitat Politecnica de Valencia, Spain (Ayudas para primeros proyectos de investigacion PAID06-06).Ávila Reséndiz, C.; Guardiola Barcena, JL.; González Nebauer, S. (2012). Response of the photosynthetic apparatus to a flowering-inductive period by water stress in Citrus. Trees - Structure and Function. 26(3):833-840. https://doi.org/10.1007/s00468-011-0657-4S833840263Addicott FT (1982) Abscission. University of California Press, BerkeleyBajji M, Kinet JM, Lutts S (1998) Salt stress effects on roots and leaves of Atriplex halimus L. and their corresponding callus. Plant Sci 137:131–142Barbera G, Fatta-del-Bosco G, Lo-Cascio B (1985) Effect of water stress on lemon summer bloom: the Forzatura technique in the Sicilian citrus industry. Acta Hortic 171:391–397Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Cassin J, Bourdeaut A, Fougue V, Furon V, Gaillard JP, LeBourdelles J, Montagut G, Moreuil C (1969) The influence of climate upon blooming of Citrus in tropical areas. Proc Int Soc Citrus 1:315–323Castel JR, Buj A (1990) Response of Salustiana oranges to high frequency deficit irrigation. Irrig Sci 11:121–127Chaikiatitiyos S, Menzel CM, Rasmussen TS (1994) Floral induction in tropical fruit trees: effects of temperature and water supply. J Hortic Sci 69:397–415Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560Costa JM, Ortuño MF, Chaves M (2007) Deficit irrigation as a strategy to save water: physiology and potential application to horticulture. J Integr Plant Biol 49:1421–1434Davenport TL (1990) Citrus flowering. Hortic Rev 12:249–408Davies FS, Albrigo LG (1994) Citrus. CAB International, Wallingford, pp 126–134Domingo R, Ruiz-Sánchez MC, Sánchez-Blanco MJ, Torrecillas A (1996) Water relations, growth and yield of Fino lemon trees under regulated deficit irrigation. Irrig Sci 16:115–123Erismann ND, Machado EC, Tucci MLS (2008) Photosynthetic limitation by CO2 diffusion in drought stressed orange leaves on three rootstocks. Photosynth Res 96:163–172Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127:343–352Gallé A, Florez-Sarasa I, Tomas M, Pou A, Medrano H, Ribas-Carbó M, Flexas J (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? J Exp Bot 60:2379–2390Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterrenean plants with different growth forms. New Phytol 175:81–93García-Luis A, Kanduser M, Santamarina P, Guardiola JL (1992) Low temperature influence on flowering in Citrus. The separation of inductive and bud dormancy releasing effects. Physiol Plant 86:648–652García-Sánchez F, Syvertsen JP, Gimeno V, Botía P, Pérez-Pérez JG (2007) Responses to flooding and drought stress by two citrus rootstock seedlings with different water-use efficiency. Physiol Plant 130:532–542Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Gómez-Cadenas A, Tadeo FR, Talon M, Primo-Millo E (1996) Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol 112:401–408Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Glob Chang Biol 16:1082–1106Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–190Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station Circular no. 347, p 32IPCC (2001) Climate change 2001. In: Houghton JT (ed) The scientific basis. Cambridge University Press, CambridgeLawlor DW (1995) The effects of water deficit on photosynthesis. In: Smirnoff N (ed) Environment and plant metabolism. Bios Scientific Publishers, Oxford, pp 129–160Lichtenthaler HK, Buschmann C (2001) Current protocols in food analytical chemistry, F4.2.1 and F4.3.1. John Wiley and Sons, Inc, NJLorimer GH, Badger MR, Andrews TJ (1977) D-Ribulose-1, 5-bisphosphate carboxilase-oxigenase. Improved methods for activation and assay of catalytic activities. Anal Biochem 78:66–75Miyashita K, Tanakamaru S, Maitani T, Kimura K (2005) Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ Exp Bot 53:205–214Nir I, Leshem B, Goren R (1972) Effects of water stress, gibberellic acid and 2-chloroethylammoniumchloride (CCC) ob flower differentiation in Eureka lemon trees. J Am Soc Hortic Sci 97:774–778Peñarrubia L, Moreno J (1988) Ribulose 1, 5-bisphosphate carboxylase oxygenase from citrus leaves. Phytochemistry 27:1999–2004Pérez-Pérez JG, Syvertsen JP, Botía P, García-Sánchez F (2007) Leaf water relations and net gas exchange responses of salinized carrizo citrange seedlings during drought stress and recovery. Ann Bot 100:335–345Pérez-Pérez JG, Robles JM, Tovar JC, Botía P (2009) Response to drought and salt stress of lemon ‘Fino 49’ under field conditions: water relations, osmotic adjustment and gas Exchange. Sci Hortic 122:83–90Reynolds M, Tuberosa R (2008) Translational research impacting on crop productivity in drought-prone environments. Curr Opin Plant Biol 11:171–179Ruiz-Sánchez MC, Domingo R, Savé R, Biel C, Torrecillas A (1997) Effects of water stress and rewatering on leaf water relations of lemon plants. Biol Plant 39:623–631Sarris D, Christodoulakis D, Körner C (2007) Recent decline in precipitation and tree growth in the eastern Mediterranean. Glob Chang Biol 13:1187–1200Sharkey TD (1990) Water-stress effects on photosynthesis. Photosynthetica 24:651Southwick SM, Davenport TL (1986) Characterization of water stress and low temperature effects on flower induction in Citrus. Plant Physiol 81:26–29Spiegel-Roy P, Goldschmidt EE (1996) Biology of Citrus. Cambridge University Press, Cambridge, pp 131–136Syvertsen JP, Lloyd J (1994) Citrus. In: Schaffer BA, Andersen PC (eds) Handbook of environmental physiology of fruit crops. Vol II Subtropical and tropical crops. CRC Press, Boca Raton, pp 65–99Syvertsen JP (1996) Water stress and carbon budgets. Proc Int Soc Citrus 1:46–50Valladares F, Arrieta S, Aranda I, Lorenzo D, Sánchez-Gómez D, Tena D, Suarez F, Pardos JA (2005) Shade tolerance, photoinhibition sensitivity and phenotypic plasticity of Illex aquifolium in continental Mediterranean sites. Tree Physiol 25:1041–1052Vu JCV, Yelenosky G (1988) Solar irradiance and drought stress effects on the activity and concentration of ribulose bisphosphate carboxylase in ‘Valencia’ orange leaves. Isr J Bot 37:245–25

Signal processing and transduction in plant cells: the end of the beginning?

Plants have a very different lifestyle to animals, and one might expect that unique molecules and processes would underpin plant-cell signal transduction. But, with a few notable exceptions, the list is remarkably familiar and could have been constructed from animal studies. Wherein, then, does lifestyle specificity emerge

Partner choice through concealed floral sugar rewards evolved with the specialization of ant–plant mutualisms

SummaryObligate mutualisms require filtering mechanisms to prevent their exploitation by opportunists, but ecological contexts and traits facilitating the evolution of such mechanisms are largely unknown. We investigated the evolution of filtering mechanisms in an epiphytic ant-plant symbiotic system in Fiji involving Rubiaceae and dolichoderine ants, using field experiments, metabolomics, X-ray micro-computed tomography (micro-CT) scanning and phylogenetics. We discovered a novel plant reward consisting of sugary sap concealed in post-anthetic flowers only accessible to Philidris nagasau workers that bite through the thick epidermis. In five of the six species of Rubiaceae obligately inhabited by this ant, the nectar glands functioned for 10 d after a flowerandapos;s sexual function was over. Sugar metabolomics and field experiments showed that ant foraging tracks sucrose levels, which only drop at the onset of fruit development. Ontogenetic analyses of our focal species and their relatives revealed a 25-fold increase in nectary size and delayed fruit development in the ant-rewarding species, and Bayesian analyses of several traits showed the correlated evolution of sugar rewards and symbiosis specialization. Concealed floral nectar forestalls exploitation by opportunists (generalist ants) and stabilizes these obligate mutualisms. Our study pinpoints the importance of partner choice mechanisms in transitions from facultative to obligate mutualisms.</p