Proteome-wide response of dormant caryopses of the weed, Avena fatua, after colonization by a seed-decay isolate of Fusarium avenaceum

Authors: LEWIS, RICKY - Washington State University; Okubara, Patricia; SULLIVAN, TARAH - Washington State University; MADDEN, BENJAMIN - Mayo Clinic; JOHNSON, KENNETH - Mayo Clinic; CHARLESWORTH, CRISTINE - Mayo Clinic; FUERST, E - Washington State University

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2021
Publication Date: 5/1/2022
Citation: Lewis, R.W., Okubara, P.A., Sullivan, T.S., Madden, B.J., Johnson, K.L., Charlesworth, C.M., Fuerst, E.P. 2022. Proteome-wide response of dormant caryopses of the weed, Avena fatua, after colonization by a seed-decay isolate of Fusarium avenaceum. Phytopathology. 112(5):1103-1117. https://doi.org/10.1094/PHYTO-06-21-0234-R.
DOI: https://doi.org/10.1094/PHYTO-06-21-0234-R

Interpretive Summary: Yield reduction in wheat agroecosystems is exacerbated by the accumulation of wild oat seeds in the soil. Wild oat competes with wheat for nutrients and water, especially in soils undergoing heavy metal release due to acidification. The soilborne fungal pathogen causing Fusarium root and crown of small-grain cereals preferentially caused seed decay in wild oat compared to wheat. This objective of this research was to examine the interaction between the weed seeds and the weed pathogen at the protein level. The findings indicated that defense response proteins are induced in wild oat seeds during infection with the decay pathogen, and that the pathogen itself produced defense proteins in the presence of wild oat seeds. This complex interaction needs to be untangled in order to develop new biocontrol strategies for weed seed management.

Technical Abstract: Agronomic weed pressure presents a major hurdle to worldwide crop production, with wild oat (Avena fatua) being considered a prominent pest plant in many production systems, including wheat (Triticum aestivum) cropping regions. Because Fusarium avenaceum F.a.1 preferentially decays A. fatua caryopses compared with T. aestivum caryopses, examining the interaction between A. fatua and F. avenaceum F.a.1 may provide novel insights into crucial molecular mechanisms regulating the decay of this important weed species. While single enzyme assays have revealed the importance of specific defense enzymes during caryopsis-fungus interactions, there is a lack of information regarding the broader proteomic response. The primary objective of this proteomics study was to obtain a more global perspective of proteins expressed in caryopses or caryopsis leachates (soluble proteins) after colonization by F. avenaceum F.a.1. Because soil acidification and associated metal toxicity are a growing agricultural issue, the influence of aluminum (Al) on the proteomic response of A. fatua to F.a.1 was examined. After three days of caryopsis-fungus interaction in the absence or presence of Al, the proteomic response of A. fatua was observed in both caryopsis leachates and whole caryopses, with leachates only being examined in the absence of Al. The findings show that fungal colonization results in global proteomic changes in the caryopsis leachates, including induction of plant proteins related to primary metabolism, secondary metabolism, cell structure, cellular processes, development, defense/stress, and signaling. Additionally, leachates were heavily enriched in fungal proteins related to various processes, including these same functional categories along with pathogenicity. In whole caryopsis samples, fungal colonization in the absence of Al resulted in induction of Pathogenesis-related proteins 1 and Actin-1, and repression Late embryogenesis abundant protein (group 3), and ABA-inducible protein PHV A1-Like. In the presence of Al, fungal colonization resulted in induction of Pathogenesis-related protein 1, and repression of ABA-inducible protein PHV A1-like, Histone H1, and 16.9 kDa class I heat shock protein 3 (which was induced in the presence of Al but in the absence of fungal colonization). Overall, Al had little detectable impact on whole caryopsis-fungal interactions, which could be a result of the low relative abundance of proteins in wild oat seeds coupled with the high abundance of fungal proteins (which could mask the treatment effect). Ultimately, the results show that caryopsis leachates are a rich resource to investigate the proteome of both plant hosts and fungal pathogens, and that the interaction results in global proteome changes in the host.