Research articleMagnesium decreases leaf scald symptoms on rice leaves and preserves their photosynthetic performance
Introduction
Among the diseases affecting rice production worldwide, leaf scald, caused by the fungus Monographella albescens [(Hashiola and Yokogi) Samuels and I. C. Hallet = Rhynchosporium oryzae Hashiola and Yokogi], is one of the greatest importance (Filippi et al., 2005). On leaves, leaf scald symptoms appear as zonate or oblong colored olive lesions with light brown halos without well-defined margins (Filippi et al., 2005). As the disease develops, large part of the leaf blades become blight and dry out very quickly giving the leaf a scalded appearance (Ou, 1985, Nunes et al., 2004, Filippi et al., 2005).
Magnesium (Mg) is the central atom in the tetrapyrrole ring of both chlorophyll (Chl) a and Chl b molecules in the chloroplasts in order to make effective at gathering light for photosynthetic carbon reduction reactions (Taiz and Zeiger, 2009). The Mg per se is also involved in CO2 assimilation reactions (Hannaway et al., 1980) as the photophosphorylation reactions that occur in the chloroplasts are affected by the Mg ions (Marschner, 1995). Furthermore, a large proportion (i.e., 75%) of the Mg in the leaf cells is associated either directly or indirectly with the protein synthesis, via its roles in ribosomal structure and function, for the stability of ribosomal particles (Bould et al., 1984, Marschner, 1995). The Mg is also required for RNA polymerase activity and thus for the formation of RNA in the nucleus (Marschner, 1995). Also, mitochondria in plant cells undergo structural degeneration without adequate amounts of Mg (Marinos, 1963). This may occur because many respiratory enzymes such as the phosphatases, ATPases and carboxylases require Mg (Marschner, 1995). Thus, Mg plays a central role in ATP and energy metabolism. Considering that Mg is preferentially bound to phosphoryl groups, it forms an Mg-ATP complex, which can be used by the active sites of ATPases for transferring energy-rich phosphoryl groups (Marschner, 1995). Finally, besides being required for the activation of several enzymes involved in lipid metabolism (e.g., acetic thiokinase and various phospholipid-synthesizing enzymes), Mg is also involved in the biosynthesis of phospholipids, and therefore, in the formation of functional cell membranes (Marschner, 1995).
The understanding of physiological changes that occur in a certain host during the infection process of a pathogen allows us to predict the effects of the disease on both crop growth and yield (Boote et al., 1980, Bastiaans, 1993). Plant growth and photosynthesis are negatively impacted due to the infection of pathogens associated with irreversible damages to the photosynthetic apparatus (Bassanezi et al., 2002, Berger et al., 2004; Dan Gao et al., 2011, Iqbal et al., 2012, Resende et al., 2012; Aucique-Pérez et al., 2014, Debona et al., 2014). Therefore, the proper assessment of the photosynthetic performance of plants infected by pathogens through the simultaneous measurement of leaf gas exchange and Chl a fluorescence parameters can provide crucial insights into the mechanisms underlying their intrinsic interaction with the potential to obtain new control strategies for the disease (Berger et al., 2007, Rolfe and Scholes, 2010). A decrease in the net carbon assimilation rate as well as limitations on stomatal and mesophyll conductance are the primary effects caused by pathogens infection (Berger et al., 2007, Barón et al., 2012). Taking this into consideration, non-invasive methods such as Chl a fluorescence imaging, particularly when combined with leaf gas exchange measurements, can provide a detailed spatio-temporal analysis of how an infected leaf may respond to a certain pathogen infection (Baker et al., 2001, Rolfe and Scholes, 2010, Iqbal et al., 2012, Rousseau et al., 2013, Tatagiba et al., 2015). Indeed, the Chl a fluorescence imaging technique has successfully been used in a range of studies to assess the interactions between plants and fungal pathogens (Rolfe and Scholes, 2010). This technique provides images that map the changes in single parameters associated with photosynthesis onto the leaves (Rousseau et al., 2013). Among the various Chl a fluorescence parameters that can be measured, the maximum photosystem (PS) II photochemical quantum efficiency, often assessed by the variable-to-maximum Chl a fluorescence ratio (Fv/Fm), has widely been used to compare non-infected and infected host tissues (Rousseau et al., 2013, Tatagiba et al., 2015). This ratio is close to or slightly above 0.8 in non-infected leaf tissue and progressively decreases as the damages to the PS II reaction centers are exacerbated (Krause and Weis, 1991). By comparison, the energy absorbed by PS II reaction centers can be divided between the fraction used in photochemistry [Y(II)] and that lost non-photochemically, which can be further divided into two competing non-photochemical pathways: the yield induced by down-regulatory processes [Y(NPQ)] associated with controlled thermal dissipation and the yield for other energy losses [Y(NO)] (Kramer et al., 2004). The measurement of the Y(NPQ) parameter give us an estimate of the level of photon flux density shows, therefore, that the leaf has retained the physiological means to protect itself by regulation (Kramer et al., 2004). On the other hand, the Y(NO) parameter indicates that both photochemical energy conversion and protective regulatory mechanisms are inefficient (Kramer et al., 2004). In general, during the infection process of the most aggressive pathogens in the absence of the appearance fo disease symptoms, the values of the parameters Y(II), Y(NPQ) and Fv/Fm decrease while the values of Y(NO) increase (Rolfe and Scholes, 2010, Resende et al., 2012, Aucique-Pérez et al., 2014, Debona et al., 2014, Tatagiba et al., 2015, Jiao et al., 2016). Depending on the host-pathogen interaction, the concentration of Mg on the plant tissue can decrease or increase the resistance to diseases (Huber, 1981). For example, a high foliar concentration of Mg exacerbated disease symptoms on the leaves of tomato and green pepper infected with Xanthomonas campestris pv. vesicatoria (Woltz and Jones, 1979). In sharp contrast, a high concentration of Mg on rice leaf sheaths was associated with reduced size of the lesions of sheath blight caused by Rhizoctonia solani (Schurt et al., 2014). Moreira et al. (2013) also reported that high foliar Mg concentration reduced the severity of brown spot on rice and increased the activities of polyphenoloxidases, peroxidases and phenylalanine ammonia-lyases. From the above, whether and how a proper Mg concentration on leaf blades can alter host resistance to diseases remains to be fully resolved (Jones and Huber, 2007).
Considering the importance of Mg in plant metabolism and the lack of information about the effect of Mg on the rice-M. albescens interaction, especially at the photosynthesis level, the present study was carried out to perform an in-depth analysis of the photosynthetic performance of rice leaves challenged with Monographella albencens by combining leaf gas exchanges, Chl a fluorescence images and photosynthetic pigment analyses.
Section snippets
Nutrient solution preparation and plant growth
Rice plants were grown in nutrient solutions prepared based on Hoagland and Arnon (1950) with some modifications and consisted of: 1.0 mM KNO3, 0.25 mM NH4H2PO4, 0.1 mM NH4Cl, 1.0 mM Ca(NO3)2, 0.30 μM CuSO4.5H2O, 0.33 μM ZnSO4.7H2O, 11.5 μM H3BO3, 3.5 μM MnCl2.4H2O, 0.1 μM (NH4)6Mo7O24.4H2O, 25 μM FeSO4.7H2O and 25 μM EDTA disodium. The Mg doses were 0.5 mM (using MgSO4.7H2O) or 1.5 mM (0.5 mM in the form of MgSO4.7H2O and 1.0 mM in the form of MgCl2). These two Mg doses were chosen based on
Foliar Mg concentration
The foliar Mg concentration significantly decreased by 20 and 23%, respectively, for the non-inoculated and inoculated plants as the Mg doses decreased from 1.5 to 0.5 mM (Fig. 1).
Lesion length
Significant increases of 12, 13 and 14% at 72, 96 and 120 hai, respectively, in the lesion size occurred for plants supplied with 0.5 mM of Mg (hereafter referred to as –Mg plants) in comparison to those that received 1.5 mM of Mg (hereafter referred to as + Mg plants). At 120 hai, the lesions on the leaves of –Mg
Discussion
In this study, the Mg treatments resulted in leaf Mg concentrations (values ranging from 0.55 to 0.84 dag/kg) that are within or slightly greater than those that are believed as normal Mg levels in rice leaves which vary from 0.50 to 0.70 dag/kg (Malavolta et al., 1997). To the best of our knowledge, this current study provides the first evidence that a proper foliar Mg concentration is of utmost importance to decrease the leaf scald symptoms in addition to partially preserving the
Contribution
S. D. Tatagiba was responsible for design and conducting the experiments as well as preparation of the manuscript.
F. M. DaMatta and F. A. Rodrigues were responsible for planning, analysis of data and preparation of the manuscript.
Acknowledgments
Profs. F. M. DaMatta and F. A. Rodrigues thank the National Council for Scientific and Technological Development (CNPq) for their research fellowship. Dr. S. D. Tatagiba was supported by CAPES. The authors thank Profa. Gisele B. Silva and Dr. Marta Cristina Corsi Filippi for their technical assistance. This study was supported by CAPES, CNPq and FAPEMIG.
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