Weed Science

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Weed Science 54(3):575-587. 2006
doi: 10.1614/WS-05-055R.1

Do microorganisms influence seed-bank dynamics?

Joanne C. Chee-Sanforda, Martin M. Williams IIb, Adam S. Davisb, and Gerald K. Simsb

aCorresponding author. United States Department of Agriculture—Agricultural Research Service, Invasive Weed Management Research, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801;

bUnited States Department of Agriculture—Agricultural Research Service, Invasive Weed Management Research, University of Illinois, 1102 S. Goodwin Ave., Urbana, IL 61801

Abstract

Reduction of seed-bank persistence is an important goal for weed management systems. Recent interest in more biological-based weed management strategies has led to closer examination of the role of soil microorganisms. Incidences of seed decay with certain weed species occur in the laboratory; however, their persistence in soil indicates the presence of yet-unknown factors in natural systems that regulate biological mechanisms of seed antagonism by soil microorganisms. A fundamental understanding of interactions between seeds and microorganisms will have important implications for future weed management systems targeting seed banks. Laboratory studies demonstrate susceptibility to seed decay among weed species, ranging from high (velvetleaf) to very low (giant ragweed). Microscopic examinations revealed dense microbial assemblages formed whenever seeds were exposed to soil microorganisms, regardless of whether the outcome was decay. Microbial communities associated with seeds of four weed species (woolly cupgrass, jimsonweed, Pennsylvania smartweed, and velvetleaf) were distinct from one another. The influence of seeds on microbial growth is hypothesized to be due to nutritional and surface-attachment opportunities. Data from velvetleaf seeds suggests that diverse assemblages of bacteria can mediate decay, whereas fungal associations may be more limited and specific to weed species. Though microbial decay of seeds presents clear opportunities for weed biocontrol, limited success is met when introducing exogenous microorganisms to natural systems. Alternatively, a conservation approach that promotes the function of indigenous natural enemies through habitat or cultural management may be more promising. A comprehensive ecological understanding of the system is needed to identify methods that enhance the activities of microorganisms. Herein, we provide a synthesis of the relevant literature available on seed microbiology; we describe some of the major challenges and opportunities encountered when studying the in situ relationships between seeds and microorganisms, and present examples from studies by the ARS Invasive Weed Management Unit.

Nomenclature:Giant ragweed, Ambrosia trifida L.; jimsonsweed, Datura stramonium L.; Pennsylvania smartweed, Polygonum pensylvanicum L.; velvetleaf, Abutilon theophrasti Medic.; woolly cupgrass, Eriochloa gracilis (Fourn) A. S. Hitchc.

Received: May 6, 2005; Accepted: March 13, 2006

Keywords: Seed–microorganism interaction, weed seed decay, soil microbiology, microbial communities, seed-bank ecology, multitrophic systems, integrated weed management



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Figure 1. Key ecological processes mediated by soil microorganisms.

Figure 2. Seed-bank dynamics of an annual weed with emphasis on the interacting relationship between above- and below-ground processes.

Figure 3. Scales of study of giant ragweed represented by (A) complex plant communities in a landscape or field, (B) patch of weeds or individual plants, (C) seed aggregates or individual seed, and (D–F) giant ragweed seed surfaces at multiple spatial scales imaged by environmental scanning electron microscopy (ESEM). Spatial scales of measure are indicated in the left arrows and potential scales of study are listed in descending order of relative size.

Figure 4. Diaspores of giant ragweed in various stages of decay. (A) intact and viable diaspore, (B) diaspore inoculated with a mixed culture associated with decay activity during enrichment cultivation experiments, (C) diaspore from a field site that appeared intact, but after bifurcation, a cross-sectional view revealed extensive embryo decay occurred, and (D) a deteriorated diaspore recovered from a field site, with only part of the pericarp and involucre remaining.

Figure 5. Environmental electron-scanning micrographs contrasting uncolonized (left panels) and microbial-colonized (right panels) seeds of giant ragweed (A and B) and velvetleaf (C and D).

Figure 6. Bacterial community profiles associated with seed surfaces following colonization of microorganisms that were derived from the same soil inoculum, and analyzed with the use of T-RFLP analysis of 16S rDNA digested with Rsa I. (A) woolly cupgrass, (B) jimsonweed, (C) Pennsylvania smartweed, and (D) velvetleaf. Each peak is a discrete DNA fragment size that may represent a unique operational taxon (species) of bacteria.

Figure 7. Cluster analysis of bacterial communities associated with decaying seeds of velvetleaf. Each symbol at the end of a branch corresponds to a terminal restriction fragment length polymorphism (T-RLFP) profile from a seed following exposure to one of four soil-derived inocula (ASSET, ASLOC, ASSWC, USSEU). The soils were obtained locally from sites around Champaign and Urbana, Illinois and were all silty clay loams (comprised of approximately 20% sand, 50% silt, 30%clay, organic matter content 4– 7%, pH 6.1–6.2) typical of the region. Seven to nine replicate seeds corresponding to each soil inoculum were analyzed. The similarities were calculated with the use of the Dice correlation coefficient, and the best tree was drawn with the unweighted pair group method with arithmetic averages (UPGMA).

table

Table 1.Decay of weed seeds following 3-mo exposure to soil microbial inocula.a

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