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Colonization of Wounded Peanut Seeds by Soil Fungi: Selectivity for Species from Aspergillus Section Flavi

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Colonization of Wounded Peanut Seeds by Soil Fungi: Selectivity for Species from Aspergillus Section Flavi University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln U.S. Department of Agriculture: Agricultural Publications from USDA-ARS / UNL Faculty Research Service, Lincoln, Nebraska 2005 Colonization of wounded peanut seeds by soil fungi: selectivity for species from Aspergillus section Flavi Bruce W. Horn USDA-ARS, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/usdaarsfacpub Horn, Bruce W., "Colonization of wounded peanut seeds by soil fungi: selectivity for species from Aspergillus section Flavi" (2005). Publications from USDA-ARS / UNL Faculty. 1565. https://digitalcommons.unl.edu/usdaarsfacpub/1565 This Article is brought to you for free and open access by the U.S. Department of Agriculture: Agricultural Research Service, Lincoln, Nebraska at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications from USDA-ARS / UNL Faculty by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Mycologia, 97(1), 2005, pp. 202±217. q 2005 by The Mycological Society of America, Lawrence, KS 66044-8897 Colonization of wounded peanut seeds by soil fungi: selectivity for species from Aspergillus section Flavi Bruce W. Horn1 Key words: a¯atoxin, Arachis hypogaea, Aspergillus National Peanut Research Laboratory, Agricultural alliaceus, Aspergillus caelatus, Aspergillus ¯avus, As- Research Service, U.S. Department of Agriculture, pergillus niger, Aspergillus parasiticus, Aspergillus ta- Dawson, Georgia 39842 marii, competitive saprophytic ability, Eupenicillium ochrosalmoneum, fungal competition, Penicillium, wa- ter activity Abstract: Soil is a source of primary inoculum for Aspergillus ¯avus and A. parasiticus, fungi that pro- duce highly carcinogenic a¯atoxins in peanuts. Af- INTRODUCTION latoxigenic fungi commonly invade peanut seeds dur- ing maturation, and the highest concentrations of af- Carcinogenic a¯atoxins produced by Aspergillus ¯a- latoxins are found in damaged seeds. A laboratory vus and A. parasiticus are common contaminants of procedure was developed in which viable peanut peanuts, corn, cottonseed and tree nuts (Diener et seeds were wounded and inoculated with ®eld soil al 1987, Payne 1998). In Africa and southeastern containing natural populations of fungi, then incu- Asia, a¯atoxins have been shown to increase the in- bated under different conditions of seed water activ- cidence of human liver cancer by acting synergisti- ity and temperature. Densities of Aspergillus section cally with hepatitis viruses (Wild and Turner 2002). Flavi in soil used for inoculating seeds were low rel- In addition to the health concerns related to a¯atox- ative to the total numbers of ®lamentous fungi ins, the cost of managing a¯atoxins is often very (,1%). Aspergillus species from section Flavi present high, averaging $26 million annually to the peanut in soil included A. ¯avus morphotypes L and S industry in the southeastern United States alone strains, A. parasiticus, A. caelatus, A. tamarii and A. (Lamb and Sternitzke 2001). alliaceus. Wounding was required for high incidences Aerial crops such as corn and cottonseed are in- of fungal colonization; viability of wounded seeds had fected predominantly with A. ¯avus, whereas peanuts little effect on colonization by Aspergillus species. (Arachis hypogaea) with their subterranean growth Peanut seeds were colonized by section Flavi species habit are invaded by both A. ¯avus and A. parasiticus as well as A. niger over broad ranges of water activity (Horn 2003). A. ¯avus has been divided into two (0.82±0.98) and temperature (15±37 C), and the morphotypes: the typical L strain that produces large highest incidences of seed colonization occurred at sclerotia .400 mm diam and the S strain, described water activities of 0.92±0.96 at 22±37 C. A. parasiticus as variety parvisclerotigenus (Saito and Tsuruta 1993), colonized peanut seeds at lower temperatures than which produces numerous small sclerotia ,400 mm A. ¯avus, and cool soil temperatures relative to tem- (Cotty 1989). Other Aspergillus species belonging to peratures of aerial crop fruits might explain why A. section Flavi have been reported from peanuts, in- parasiticus is found mostly in peanuts. Other fungi, cluding A. caelatus and A. tamarii (Horn 1997, Horn dominated by the genera Penicillium, Fusarium and and Greene 1995). Another species, A. alliaceus (te- Clonostachys, colonized seeds primarily at water activ- leomorph 5 Petromyces alliaceus), has been trans- ities and temperatures suboptimal for section Flavi ferred to section Flavi based on molecular characters species and A. niger. Eupenicillium ochrosalmoneum (Peterson 2000). None of these other species forms frequently sporulated on the conidial heads of sec- a¯atoxins, although A. tamarii produces cyclopiazon- tion Flavi species and showed speci®city for these ic acid (Horn et al 1996) and A. alliaceus produces fungi. The inoculation of wounded viable peanut ochratoxin A (Bayman et al 2002a). seeds with soil containing natural populations of fun- Soil serves as a reservoir for primary inoculum of gi provides a model system for studying the infection A. ¯avus and A. parasiticus (Horn et al 1995, Horn process, the interactions among fungi and those fac- and Dorner 1998), and peanut pods are in direct tors important in a¯atoxin formation. contact with soil populations of a¯atoxigenic fungi. Infection of peanut seeds predominantly by primary Accepted for publication 6 September 2004. inoculum differs from infection of corn and cotton- 1 E-mail: [email protected] seed in which secondary inoculum plays a dominant 202 HORN: ASPERGILLUS COLONIZATION OF PEANUT SEEDS 203 role (Horn 2003). Two modes of infection are pos- tent. The remaining soil was stored at 5 C in sealed plastic sible in peanuts. First, seeds from pods without visible bags and used within 3 wk to determine fungal population damage may be invaded by a¯atoxigenic fungi when densities and for inoculating seeds. plants are drought stressed (Sanders et al 1981), al- Fungal soil populations.ÐAspergillus species and total ®la- though undetected microscopic pod damage might mentous fungi were enumerated, and Aspergillus species account for some of this infection (Porter et al 1986). were identi®ed as described by Horn and Dorner (1998). Second, pod and seed damage allows for direct in- Brie¯y, three 3.3 g subsamples of soil were vortexed in 10 vasion from soil. The highest levels of A. ¯avus and mL of 0.2% water agar. Soil suspensions of subsamples each A. parasiticus infection and a¯atoxin contamination were dilution plated onto ®ve plates (0.2 mL/plate) of mod- are associated with seed damage (Blankenship et al i®ed dichloran-rose bengal medium and incubated 3±4 d at 37 C. Species from Aspergillus section Flavi were identi- 1984, Dowell et al 1990, Hill et al 1983, Sanders et al ®ed under a stereomicroscope directly from the dilution 1985b). Larvae of lesser cornstalk borer (Elasmopal- plates with the exception of A. caelatus and A. tamarii, pus lignosellus) scarify and penetrate peanut pods which were subcultured to Czapek agar (Cz) slants for ®nal and largely are responsible for pod and seed damage identi®cation. Aspergillus species from other sections not in the United States (Lynch 1984, Lynch and Mack recognizable on dilution plates were subcultured and iden- 1995, Lynch and Wilson 1991). In tropical regions ti®ed according to the techniques of Klich (2002) and Rap- where peanuts are cultivated, white grubs (scarab er and Fennell (1965). The density of total ®lamentous fun- beetle larvae), termites and millipedes are important gi was determined on unmodi®ed dichloran-rose bengal feeders on peanut pods (Lynch and Mack 1995). medium after 5 d at 25 C (Horn et al 1994), and those Growth cracks also may expose seeds to soil inoculum same plates were incubated an additional 2±3 d (30 C) to 5 that results in an increase in fungal invasion and af- enumerate Eupenicillium ochrosalmoneum (anamorph Penicillium ochrosalmoneum) and Eup. cinnamopurpureum latoxins (Schroeder and Ashworth 1965). (anamorph 5 Pen. cinnamopurpureum). Eupenicillium spe- Peanut seeds vary considerably in water activity cies were recognized on dilution plates by colonies domi- (Aw) and exposure to soil temperatures. Water activ- nated by ascostromata; isolates were subcultured to Cz slants ities of individual seeds range from 0.75 to 1.00 (Dor- and identi®ed according to Pitt (1979). All fungal densities ner et al 1989, JW Dorner unpublished data), and were corrected for soil moisture and were reported on a soil temperatures in the pod zone range from 20 C dry-weight basis. in warm temperate regions to .38 C in semi-arid Peanut seeds.ÐIrrigated peanut plants of the cultivar Geor- tropical areas (Craufurd et al 2003, Hill et al 1983). gia Green were grown using standard applications of fertil- Peanuts are invaded by a¯atoxigenic fungi primarily izer, herbicides, fungicides and insecticides (Guillebeau under conditions of late-season drought and elevated 2004). Peanut plants were dug from ®elds on 18 Oct 2000 soil temperatures (Blankenship et al 1984, Hill et al (7.9 km northeast of Cuthbert, Randolph County, Georgia), 1983, Sanders et al 1981, Sanders et al 1985b). 13 Sep 2001 (5.4 km southwest of Dawson, Terrell County), For this study a laboratory technique was devel- and 8 Sep 2002 and 11 Sep 2003 (2.1 km north of Sasser, oped in which viable peanut seeds were wounded Terrell County) with a digger-inverter, and pods immedi- and the wound sites were inoculated with soil from ately were hand picked. Fresh pods were abraded with a the ®eld. The effects of various factors on peanut wet-impact blaster to expose the inner pericarp wall, then seed colonization by Aspergillus section Flavi species color sorted according to maturity (Williams and Drexler 1981, Williams and Monroe 1986). Mature pods (black and from natural populations in soil, including water ac- brown maturity classes) were removed and dried 14 d at tivity, temperature, wounding and seed viability, are ambient temperature on a forced-air drier.
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