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Brassinosteroid Analogue Affects the Senescence in Two Papaya

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Brassinosteroid Analogue Affects the Senescence in Two Papaya RESEARCH ARTICLE Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress Mara de Menezes de Assis Gomes1*, Alena Torres Netto1, Eliemar Campostrini1, Ricardo Bressan-Smith1, Marco António Teixeira Zullo2, Tiago Massi Ferraz1, Luciane do Nascimento Siqueira1, Nilton Rocha Leal1, Miriam Núñez-Vázquez3 1Setor de Fisiologia Vegetal, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ, Brazil. 2Laboratório de Fitoquímica, Instituto Agronômico de Campinas, Campinas, SP, Brazil. 3Instituto Nacional de Ciencias Agrícolas, La Habana, Cuba. *Corresponding author: [email protected] Received: 20 December 2012; Accepted: 26 September 2013 ABSTRACT: Brassinosteroids (BS) application is associated with the increase of tolerance to some kinds of stresses, such as those induced by the infection of pathogens, temperature, salt and water deficiency. In this work, the influence of a spirostanic analogue of brassinosteroid (SAB) in the leaves of papaya Golden and UENF/CALIMAN 01 (UC 01) was tested to evaluate alterations in the content of chlorophyll in plants submitted to drought stress (DS). When plants were 70 d old, SAB was applied (0,1 mg L-1) for five consecutive days in half of the plants meant for the experiment. The treatments were: control irrigated (I), I with SAB (IB), DS and DS with SAB (DSB). The evaluated leaves were marked in accordance to the age: LEAF 1 (youngest expanded leaf), LEAF 2 (insertion immediately below LEAF 1) and LEAF 3 (insertion immediately below LEAF 2). The same leaves were used throughtout the experimental period. After the thirteenth day, the chlorophyll contents of DSB (Golden and UC 01) were always lesser than the treatment DS in LEAF 2. The irrigation was restarted in stressed plants on the fifteenth day, followed by new application of SAB (IB and DSB treatments). In Golden plants, DSB showed the lowest values of chlorophyll contents after re-watering, while in UC 01, differences in chlorophyll contents between treatments DS and DSB had not occurred. Alterations in Fv/Fm relation did not occur among the treatments during stress. In genotype UC 01, the irrigated plants showed minor values of Fv/Fm at the end of the experiment, whereas the plants submitted to DS presented increments in this relation in this same time. These results indicate that SAB might have contributed to accelerate the rate of leaf senescence of the oldest leaves of stressed plants, redistributing photoassimilates and other compounds for the youngest leaves. KEYWORDS: chlorophyll content, Carica papaya L., fluorescence, water relations. INTRODUCTION environmental factors (Noodén 1988, Smart 1994), including Leaf senescence is a structurally, physiologically and abiotic and biotic factors such as drought, nutrient limitation, genetically coordinated process, where organelles and their extreme temperature, and oxidative stress by UV-B irradiation constituents are sequentially broken down and the nutrients and ozone (Lim et al. 2007). released are recycled by organs that are growing actively, such Brassinosteroids (BS) are endogenous plant growth-promoting as young leaves and fruits (Noodén 1988). Leaf senescence hormones that act on plant development and affect numerous is guided by changes in gene expression. A majority of genes physiological processes at low concentrations (Mandava 1988, that are active in non-senescent leaves, such as those involved Müssig and Altmann 1999, Zullo and Adam 2002), and senescence in photosynthesis, are repressed while other genes, such is a developmentally regulated and genetically programmed as senescence-associated genes (SAGs), are upregulated process that may be mediated by brassinosteroids (Zhao et al. (He et al. 2001). Physiological and biochemical studies suggest 1990, He et al. 1996, Li et al. 1996, Clouse and Sasse 1998, that leaf senescence is regulated by certain endogenous and Vardhini and Rao 2002). Brassinosteroids induced senescence 186 Theoretical and Experimental Plant Physiology, 25(3): 186-195, 2013 Brassinosteroids and drought stress on papaya in detached cotyledons of cucumber seedlings (Zhao et al. 1990) BS regulates plant stress responses via crosstalk with other and leaves of mung bean seedlings (He et al. 1996). Additionally, hormones (Krishna 2003). Divi et al. (2010) showed that Arabidopsis mutants lacking bioactive brassinosteroids show delay ABA suppresses BR effects on thermo-tolerance, but BR may in chloroplast senescence (Li et al. 1996). Other studies involving enhance ABA responses under certain conditions by increasing brassinosteroids have emphasized the potential of these substances ABA levels. in protecting the plants against several stresses, including cold, We hypothesized that the application of BS in papaya leaves herbicides (Khripach et al. 2000), heat (Dhaubhadel et al. 2002), of plants subjected to water stress can affect the chlorophyll diseases (Nakashita et al. 2003), drought stress, low temperature content (leaf senescence) and photochemical efficiency. and salinity stress (Kagale et al. 2007). The BS increase is generally In addition, intra-specific variability at BR response in papaya correlated with higher expression of stress marker genes, such as heat genotypes subjected to progressive water stress can be verified. shock protein (hsp) genes, like RD29A and ERD10 (Dhaubhadel et al. 1999, Kagale et al. 2007), indicating that increased expression of MATERIAL AND METHODS stress-responsive genes is responsible, in part, for the higher stress tolerance in BR-treated plants (Divi et al. 2010). Experiment Conditions: Two Carica papaya genotypes, Water stress is one of the most deleterious stresses for UENF-CALIMAN (UC 01) and Golden, were planted in plants; its occurrence invariably leads to physiological changes polystyrene trays using Plantmax as a substrate. After 33 d, the like stomatal closure, leaf abscission, composition of cell wall plantlets were transferred to 10 L pots filled with soil, sand and and plasma membrane with a decline on photosynthesis and manure mixture (1:2:1). The following treatments were applied growth (Jager et al. 2008). In some instances, brassinosteroids 70 d after seedling: Irrigated control (I), irrigated control with have been suggested to confer tolerance of plant to water stress BS application (IB), drought stress (DS), and drought stress (Zhang et al. 2008, Li et al. 2008). In soybean (Glycine max L.), with BS application (DSB). The brassinosteroid used was brassinolide applied at the beginning of bloom on plants a spirostanic analogue of brassinosteroid — BIOBRAS-16 subjected to water stress, enhanced drought tolerance (Rodríguez et al. 2006), at 1 mg L-1 concentration. It was and minimized yield loss (Zhang et al. 2008). In Robinia sprayed on the leaves at 5:00 p.m. for five consecutive days pseudoacacia seedlings, soaking roots in brassinolide prior to before the drought stress treatment and on the day of rewatering planting increased the peroxidase, superoxide dismutase and (15 d after water suspension). When the available water in catalase activities in water stressed plants when compared to the substrate was below 10%, the plants subjected to drought control plants (Li et al. 2008). stress were rewatered. The leaves were marked as LEAF 1 (the Papaya (Carica papaya L.) is a semi-woody giant herb, youngest fully expanded leaf close to the apex), LEAF 2 and this species is considered to be drought sensitive and (the first mature leaf immediately below the insertion of responsive to irrigation (Carr 2013), so soil water availability LEAF 1), and LEAF 3 (the second mature leaf immediately limits many physiological processes of papaya (Marler et al. below the insertion of LEAF 2). The chlorophyll fluorescence 1994, Clemente and Marler 1996, Mahouachi et al. 2007). and relative water content measurements were carried out only The irrigation of papaya plants is recommended during dry on LEAF 1, while chlorophyll content measurements were periods to increase growth and fruit production (Malo and assayed for leaves 1, 2 and 3. For each treatment, twenty plants Campbell 2006) whereas incorrect water management can were used (eighty plants for each genotype). At the beginning adversely affect several physiological processes (Campostrini of the experiment, all the plants were uniform in leaf number and Glenn 2007, Campostrini et al. 2010). Mahouachi et al. and height. The leaves used in this experiment remained (2006, 2007, 2012) reported that papaya responds to drought exactly the same during the whole period, independent of the by decreasing plant growth and leaf gas exchange parameters appearance of younger leaves. and promoting leaf abscission. Mahouachi et al. (2007) suggest that abscisic acid (ABA) could be involved in the induction of Soil Moisture: The soil moisture (SM) was determined three several progressive responses such as the induction of stomatal times throughout the experiment (eleven and fifteen days after closure and leaf abscission to reduce papaya water loss. water withholding and nine days after rewatering). Soil samples Different plant hormones can regulate altogether the same were collected and placed into pots to obtain the fresh mass physiological process, and crosstalk between them can occur at (FM). After 72 h at 100°C, the dry mass (DM) was obtained by the level of hormone biosynthesis, signal transduction or gene weighing the pots. The percent humidity was calculated using expression (Nemhauser et al. 2006). It has been proposed that
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