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Plant Biology 8, 597-605 Research Paper 597 Light is Essential for Degradation of Ribulose-1,5-Bisphosphate Carboxylase-Oxygenase Large Subunit During Sudden Death Syndrome Development in Soybean J. Ji1, M. P. Scott1, 2, and M. K. Bhattacharyya1, 2 1 Interdepartmental Genetics Program and Department of Agronomy, Iowa State University, Ames, Iowa 50010, USA 2 USDA-ARS, Corn Insects and Crop Genetics Research Unit, Ames, Iowa 50014, USA Received: December 28, 2005; Accepted: April 3, 2006 Abstract: Fusarium solani f. sp. glycines (Fsg) has been reported MALDI-TOF-MS: matrix-assisted laser desorption-ionization to produce at least two phytotoxins. Cell-free Fsg culture fil- time-of-flight mass spectrometry trates containing phytotoxins have been shown to develop foliar TUNEL: terminal deoxynucleotidyl transferase (TdT)- sudden death syndrome (SDS) in soybean. We have investigated mediated dUTP nick end labelling the changes in protein profiles of diseased leaves caused by cell- free Fsg culture filtrates prepared from Fsg isolates. Two-dimen- sional sodium dodecyl sulfate-polyacrylamide gel electropho- resis (PAGE) was conducted to investigate the protein profiles Introduction of diseased and healthy leaves. An approximately 55 kDa pro- tein was found to be absent in diseased leaves. Matrix-assisted Sudden death syndrome (SDS) of soybean is caused by the fun- laser desorption-ionization time-of-flight mass spectrometric gal pathogen, Fusarium solani f. sp. glycines (Fsg). The fungus analyses and a database search revealed that the missing pro- has recently been renamed Fusarium virguliforme (Aoki et tein is the ribulose 1,5-bisphosphate carboxylase/oxygenase al., 2003). SDS has been detected in Argentina, Brazil, and the (Rubisco) large subunit, which is involved in carbon assimilation USA (Rupe and Hartman, 1999). In the United States, the dis- and photorespiration. This result was confirmed by Western blot ease has been reported in more than ten states and the esti- experiments. We have shown that light is essential for disap- mated average annual crop loss from the disease has been pearance of the Rubisco large subunit initiated by cell-free Fsg valued at around US$ 100 million (Wrather et al., 2001). SDS culture filtrates. The disappearance of the protein is fairly rapid development is affected by environmental factors such as rain- and occurs within 24 h, presumably due to degradation. Cell- fall, soil fertility, and planting date. It is also affected by geno- free, Fsg culture-induced degradation of the Rubisco large sub- type and soybean cyst nematode infection (Rupe et al., 1991, unit was accompanied by accumulation of reactive oxygen spe- 1993; Chang et al., 1997). cies under light conditions. Terminal deoxynucleotidyl transfer- ase-mediated nick end labelling experiments suggested that SDS is characterized by root rot, crown necrosis, premature programmed cell death was initiated in leaves of seedlings fed defoliation, and flower and pod abortion (Rupe, 1989). Fsg is a with cell-free Fsg culture filtrates. These results suggest that, in soil-borne fungal pathogen (Roy et al., 1997). In susceptible the presence of light, Fsg culture filtrates containing phytotoxins soybean cultivars, the infected roots show crown necrosis and cause degradation of the Rubisco large subunit and accumula- rotting symptoms within 2 weeks of planting. Fsg produces a tion of free radicals and, thereby, initiate programmed cell large number of asexual spores on the surface of the severely death leading to foliar SDS development in soybean. infected soybean roots. SDS foliar symptoms, also known as leaf scorch, develop slowly. About 1 or 2 months following Key words: Fusarium solani f. sp. glycines, Fusarium virguliforme, planting, interveinal chlorotic spots appear in infected sus- soybean, SDS, Rubisco, MALDI-TOF-MS, TUNEL. ceptible plants. The spots develop into necrotic or chlorotic streaks and, in the late stage, premature defoliation occurs Abbreviations: (Melgar and Roy, 1994). Fsg has never been isolated from Fsg: Fusarium solani f. sp. glycines aboveground portions of the soybean plant. The foliar symp- SDS: sudden death syndrome toms are therefore presumably induced by Fsg phytotoxins PAGE: polyacrylamide gel electrophoresis (Roy et al, 1989; Rupe, 1989; Strobel, 1982). Under greenhouse Rubisco: ribulose 1,5-bisphosphate carboxylase/ conditions, leaf scorch resistance is governed by a single gene oxygenase in the cultivar, Ripley, and by two genes in P9451 (Stephens et al., 1993; Ringler and Nickell, 1996). Under field conditions, SDS resistance is partial and governed by multiple genes (Chang et al., 1996, 1997; Hnetkovsky et al., 1996; Meksem et Plant Biol. 8 (2006): 597– 605 al., 1999; Njiti et al., 1996, 1997, 2002). Several quantitative © Georg Thieme Verlag KG Stuttgart · New York trait loci for SDS resistance have been identified (Iqbal et al., DOI 10.1055/s-2006-924175 · Published online July 5, 2006 2002; Njiti et al., 2002). ISSN 1435-8603 598 Plant Biology 8 (2006) J. Ji, M. P. Scott, and M. K. Bhattacharyya In plants, programmed cell death (PCD) is initiated during de- mec, 1995) and cause chlorosis of citrus leaves. They disrupt velopment, senescence, exposure to phytotoxins and under chloroplasts by causing chloroplast membranes to swell and stresses caused by high ozone concentration and pathogen at- by disorganizing the granule stacks (Achor et al., 1993; Nemec, tack (Buchanan et al., 2000; Greenberg, 1996; Yao et al., 2001; 1995). Pasqualini et al., 2003; Levine et al., 1996). There are several host-selective toxins that trigger PCD leading to necrosis (Wol- Cell-free culture filtrates of Fsg have been found to cause SDS pert et al., 2002). For example, victorin, a toxin produced by foliar symptoms routinely in 3-week-old seedlings and it was Cochliobolus victoriae, causes a mitochondrial oxidative burst suggested that Fsg phytotoxins translocated from roots are re- and PCD in oat (Yao et al., 2001; Navarre and Wolpert, 1999). sponsible for development of foliar symptoms (Li et al., 1999). AAL toxin produced by Alternaria alternata f. sp. lycopersici The cell-free Fsg culture filtrates can also cause cell death (Li et causes PCD and the Alternaria stem canker disease in tomato al., 1999). Cell-free culture filtrates isolated from non-patho- (Lincoln et al., 2002). AM toxins I– III, produced by the Alterna- genic F. solani isolates did not cause leaf scorch in soybean (Li ria alternata, are host-specific. AM toxins inhibit CO2 fixation et al., 1999). Most likely, Fsg toxins produce leaf scorch only in and cause leaf necrosis. Chloroplasts are the primary target of soybean. Two phytotoxins have been isolated from the cell- AM toxins that cause leaf spot disease in apple (Miyashita et free Fsg culture filtrates: monorden and a 17-kDa proteina- al., 2003). The wheat pathogen, Pyrenophora tritici-repentis, ceous toxin. Purified fractions including the 17-kDa protein secretes at least two host-selective toxins, ToxA and ToxB, en- cause browning of soybean calli and necrosis in detached soy- coded by single genes. A recent study has indicated that in tox- bean leaves (Baker and Nemec, 1994; Jin et al., 1996). The gene in-sensitive wheat lines a host factor(s) is involved in internal- encoding this proteinaceous toxin has not been isolated. The ization of ToxA into the cytoplasm and chloroplasts (Manning role of the toxin in leaf scorch development is also unknown. and Ciuffetti, 2005). The toxin causes cell death in both toxin- We have investigated changes in protein profiles that occur sensitive and insensitive wheat lines if expressed through during leaf scorch development following feeding of soybean transformation procedures. The mechanism used by the toxin seedlings with cell-free Fsg culture filtrates. We have observed to cause disruption in the thylakoid structure is, however, not that the Rubisco large subunit is degraded in diseased leaves. yet known. Light is essential for the degradation of Rubisco large subunit by the cell-free Fsg culture filtrates. Data presented in this pa- Light is known to play an important role in activating phyto- per suggest that, in the presence of light, Fsg-specific toxin(s) toxins. Cercosporin is maintained in inactive form in fungi causes degradation of Rubisco large subunit and accumulation but, after being released from the fungal hyphae, it is oxidized of free radicals, which presumably cause PCD and leaf scorch to acquire photodynamic activity (Daub et al., 1992). Cerco- development in soybean. spora toxins, Cebetin A and B inhibit the plasma membrane and chloroplast ATPases of sugar beet in a light-dependent Materials and Methods manner (Jalal et al., 1992). The F. solani toxin, dihydrofusaru- bin, causes the degradation of tobacco leaf pigments in a Preparation of fungal culture filtrates light-dependent manner (Heiser et al., 1998, and references therein). In spinach, dihydrofusarubin causes the formation of Fusarium solani f. sp. glycines isolates Clinton and Scott were reactive oxygen species (ROS), such as superoxide, by inter- grown and maintained on solid Bilay medium (0.1% KH2PO4 rupting the photosynthetic electron transport chain of chloro- [w/v], 0.1% KNO3 [w/v], 0.05% MgSO4 [w/v], 0.05% KCl [w/v], plasts (Albrecht et al., 1998). 0.02% starch [w/v], 0.02% glucose [w/v], and 0.02% sucrose [w/v]) for 12 days at 23 8C in the dark. Forty plugs were trans- Tentoxin, produced by Alternaria alternata, inhibits photo- ferred into 100 ml modified Septoria medium (MSM) and incu- phosphorylation by binding to the chloroplast ATPase. This bated for 12 days without shaking at 23 8C in the dark (Song et leads to decreased CO2 fixation and an increased number of al., 1993). Cultures were filtered through two layers of What- free electrons that cause ROS generation (Pinet et al., 1996). man No.1 filter paper and the pH was adjusted to 6.0 with Tabtoxin, produced by Pseudomonas syringae pv. tabaci, causes HCl. The cultures were refiltered through a 0.45-mm stericup chlorotic lesions in tobacco leaves in a light-dependent man- and then through a 0.22-mm stericup (Millipore, Inc.) and the ner (Durbin, 1981).
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