Phenylpropanoids are secondary metabolites ultimately synthesized from the aromatic amino acid phenylalanine (Phe; Gilchrist and Kosuge, 1980). It has been reported that adequate induction of the phenylpropanoid pathway within the first three weeks post-germination can influence a plant's ability to respond to or protect itself from stresses occurring later in the life cycle (Liu et al., 1995; Bilger et al., 2001; Sullivan et al., 2003), but until recently, there were few clues as to how this actually was achieved or how it was regulated. Cosio and McClure (1984) reported that key enzymes of the flavonoid biosynthetic pathway were greatly reduced in activity by completion of leaf expansion, confirmed by recent work in assessing impact of ultraviolet-B (UV-B) on seedlings (Sullivan et al., 2007). Warpeha et al. (2008) reported that the developmental state and adequate Phe synthesis was critical for protection from UV radiation in the genetic model of Arabidopsis. Hence, it is important to fully investigate and understand how seedlings in general perceive and prepare for stress in the process of germination and exposure to UV. Herein we discuss how soybean seedlings respond to small doses of UV-B radiation in the first few weeks of growth, and assess some of the qualitative responses.
Environmental assessments over the last ten years indicate incident UV radiation has increased, even at temperate latitudes (Ajavon et al., 2003). Chronic exposure to UV light, especially UV-B (290 nm - 320 nm) radiation, causes a number of deleterious effects to land plants which have been documented in crops and uncultivated species, including reduced photosynthetic capacity, biomass yield, nutritional quality of the seed, altered patterns of species competition, plant ultrastructure and pigment production, and increased incidence of disease (reviewed in Caldwell and Flint, 1994; Stapleton et al., 1997; Grammatikopoulos et al., 1998; Sullivan and Rozema, 1999; Ries et al., 2000; Caldwell et al., 2003; reviewed in Frohnmeyer and Staiger, 2003; Sullivan, 2005; Jenkins and Brown, 2007; reviewed in Caldwell et al., 2007).
Understanding how young seedlings respond to initial exposure to UV is very important to understanding this stress. There is a wide variation in sensitivity to UV between species and among varieties of the same species (Sato et al., 1994; Torabinejad and Caldwell, 2000; Cartwright et al., 2001; Li et al., 2003; Koti et al., 2005; Rozema et al., 2005; Koti et al., 2007; Sullivan et al., 2007). It is unknown what mechanisms of perception and signal transduction determine the level of sensitivity to UV-B. The pathways that invoke "protective" responses also remain largely unstudied and undetermined (Ulm and Nagy, 2005; Sullivan et al., 2007), although G proteins are involved in the early sensing mechanism of both low fluencies of UV-A and UV-B in the genetic model Arabidopsis (Warpeha et al., 2008).
Ultraviolet radiation elicits several types of responses in higher plants. One is to initiate repair of negative alterations after the absorption and damage to DNA by UV, where UV-B exposure is followed by the repair of UV-induced thymidine dimers, as assisted by blue light (BL) (reviewed in Jansen et al., 1998; Frohnmeyer and Staiger, 2003). Plants can also prevent injury from exposure to UV-B by synthesizing and / or deploying UV screening pigments that are originally made from Phe in a pathway called the phenylpropanoid pathway. In most plants, exposure to UV-B results in the increased accumulation or new synthesis of pigments capable of directly screening UV wavelengths (Robberecht and Caldwell 1978; Li et al., 1993; Stapleton and Walbot, 1994; Caldwell et al., 1995; Landry et al., 1995; Christie and Jenkins, 1996; Gonzalez et al., 1996; Reuber et al., 1996; Rozema et al., 1997; Burchard et al., 2000; Mazza et al., 2000; Tattini et al., 2000; Bieza and Lois, 2001; Rozema et al., 2002; Weinig et al., 2004; Casati and Walbot, 2005). Ultraviolet-B can also regulate a number of gene families, particularly those associated with the phenylpropanoid pathway, including enzymes directing the production of screening pigments like chalcone synthase (CHS) (Strid et al., 1994; Liu and McClure, 1995; reviewed in Frohnmeyer and Staiger, 2003; Oravecz et al., 2006; Blanding et al., 2007; Kaiserli and Jenkins, 2007).
Additional phenylpropanoids important for protection include materials such as suberin and other structural products that are deployed by plants to build and fortify the cuticle (Bird and Gray, 2003). Exposure to UV irradiation results in an increase in the quantity of wax occurring on the surface of leaves (Gonzalez et al., 1996; Long et al., 2003). Waxes and other cuticular materials can provide protection from UV radiation (Sieber et al., 2000; Long et al., 2003) and other stresses (Kim et al., 2007; reviewed in Nawrath, 2006) in higher plants, but do depend upon attaining a particular developmental state of the seedling. Seedlings that are null mutants for the prephenate dehydratase 1 (PD1 or called ADT3 for arogenate dehydratase3) gene in Arabidopsis are unable to synthesize and deploy normal wax materials on the cotyledon, and do not form a proper cuticle. Inability to form proper cuticle and normal cuticular structures is correlated with sensitivity to UV radiation (Sieber et al., 2000; Long et al., 2003; Warpeha et al., 2008). It is also interesting to note that PD1 mutants had considerable delay in development of the chloroplast—a key difference compared to wild type seedlings. The PD1 mutants could not be induced to make Phe by the normal mechanisms (i.e., BL or UV).
Phe is an aromatic amino acid required for protein synthesis in primary metabolism, but is also the precursor to the thousands of secondary metabolites produced from the phenylpropanoid pathway (Hahlbrock and Scheel, 1989; Chapple et al., 1994; Kliebenstein 2004). Exposure to UV-B can result in the induction of genes encoding enzymes in the phenylpropanoid pathway (e.g., phenylalanine ammonia lyase (PAL) or CHS) which can affect the levels of various pigments. Expression of these genes and the activity of the encoded enzymes depend on intensity and the wavelengths of the incident UV (Margna, 1977; Chappell and Hahlbrock, 1984; Beerhues et al., 1988; Ohl et al., 1989; Li et al., 1993; Christie et al., 1994; Leyva et al., 1995; Liu and McClure, 1995; Fuglevand et al., 1996; Frohnmeyer et al., 1997; Wade et al., 2001; Brown et al., 2005; Kaiserli and Jenkins, 2007; Brown and Jenkins, 2008). For years it was unclear what controlled the synthesis of phenylpropanoids, but more recent data clearly indicate that the synthesis of Phe appears to be the rate-limiting step; i.e., the bottleneck for all downstream compounds produced in this pathway. Warpeha et al. (2006; 2008; 2009) demonstrated that in response to BL, abscisic acid, or UV, Phe is the rate-limiting step for phenylalanine-derived pigment synthesis in etiolated seedlings of Arabidopsis, and also appears to be important in soybean (Warpeha et al., 2006; 2008; 2009). Phe can account for a significant proportion of the dry mass of a plant (Lewis and Yamamoto, 1989; Margna et al., 1989; Davin and Lewis, 1992; Van Heerden et al., 1996). There is generally a small pool of Phe in seeds and in the developing young seedlings. The actual process of germination and establishment of the seedling places a heavy demand on this pool (Margna, 1977; Margna et al., 1989), whereby incidents of stress or the actual growth process necessitate an even greater demand.
Studies on Phe synthesis and the effects on primary and secondary metabolites early in development are very rare. In Arabidopsis, where the process has been examined, BL and UV induce synthesis of Phe in etiolated Arabidopsis seedlings, occurring within minutes through the activation of a signal transduction chain consisting of GCR1 (a putative G-protein coupled receptor), and GPA1 (the sole Ga-subunit coded for in the Arabidopsis genome). This activation results in the activation of PD1 (aka ADT or AT3; one of six members of the PD gene family coded for in the Arabidopsis genome and the only member expressed in the etiolated seedling). Phe production occurs as a direct result of the activation of PD1 via its physical interaction with activated GPA1 (Warpeha et al., 2006). We do not know if other plants have the same sort of dependence on Phe early in development as Arabidopsis, the model system, but it is possible that rice and soybean may have a highly similar system of regulation (Yamada et al., 2008; Warpeha et al., 2009, respectively).
Given that Phe is very important for early synthesis of primary growth of young seedlings, and given that Phe is the first metabolite required for the activation of the phenylpropanoid pathway, a priority in research is to analyze the effects of UV radiation quality on the very early stages of seedling growth and to develop a stress model to understand how crop plants use Phe early in development.
Soybean has tremendous economic importance both as a domestic, and as an export crop. It is a potent source of oil and protein, and since it can fix atmospheric nitrogen and thereby add nitrogen to the soil, it is the ideal rotation crop for maize or wheat. However, soybean is susceptible to injury by UV radiation (Biggs et al., 1981; Teramura and Murali, 1986; Teramura et al., 1990; Teramura and Sullivan, 1991; Reed et al., 1992; Mazza et al., 2000; Li et al., 2003; Gritz et al., 2005; Koti et al., 2005; Middleton et al., 2005; Koti et al., 2007; Warpeha et al., 2009). Responses to UV can vary among plant species intraspecifically, and dependent on the developmental stage of growth when UV was received (Biggs et al., 1981; Teramura and Murali, 1986; Teramura and Sullivan, 1987; Sullivan and Teramura, 1988; Reed et al., 1992; Sullivan et al., 2007). Atmospheric ozone levels are not expected to improve in the next decade(s), and the levels of incident UV radiation may thus continue to increase.
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