Detoxification of Fusaric Acid by the Soil Microbe Mucor rouxii

Article abstract of DOI:10.1021/acs.jafc.7b01655

Fusarium oxysporum f. sp. vasinfectum race 4 (VCG0114), which causes root rot and wilt of cotton (Gossypium hirsutum and G. barbadense), has been identified recently for the first time in the western hemisphere in certain fields in the San Joaquin Valley of California. This pathotype produces copious quantities of the plant toxin fusaric acid (5-butyl-2-pyridinecarboxylic acid) compared to other isolates of F. oxysporum f. sp. vasinfectum (Fov) that are indigenous to the United States. Fusaric acid is toxic to cotton plants and may help the pathogen compete with other microbes in the soil. We found that a laboratory strain of the fungus Mucor rouxii converts fusaric acid into a newly identified compound, 8-hydroxyfusaric acid. The latter compound is significantly less phytotoxic to cotton than the parent compound. On the basis of bioassays of hydroxylated analogues of fusaric acid, hydroxylation of the butyl side chain of fusaric acid may affect a general detoxification of fusaric acid. Genes that control this hydroxylation may be useful in developing biocontrol agents to manage Fov.

Full text of DOI:10.1021/acs.jafc.7b01655

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
Subscriber access provided by Binghamton University | Libraries
Article
Detoxification of Fusaric Acid by the Soil Microbe Mucor rouxii
Frankie K. Crutcher, Lorraine S. Puckhaber, Alois A. Bell, Jinggao
Liu, Sara E. Duke, Robert D. Stipanovic, and Robert L. Nichols
J. Agric. Food Chem., Just Accepted Manuscript • Publication Date (Web): 24 May 2017
Downloaded from http://pubs.acs.org on May 27, 2017
Just Accepted
“Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted
online prior to technical editing, formatting for publication and author proofing. The American Chemical
Society provides “Just Accepted” as a free service to the research community to expedite the
dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts
appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been
fully peer reviewed, but should not be considered the official version of record. They are accessible to all
readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered
to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published
in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just
Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor
changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers
and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors
or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Journal of Agricultural and Food Chemistry is published by the American Chemical
Society. 1155 Sixteenth Street N.W., Washington, DC 20036
Published by American Chemical Society. Copyright © American Chemical Society.
However, no copyright claim is made to original U.S. Government works, or works
produced by employees of any Commonwealth realm Crown government in the course
of their duties.

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
Page 1 of 19
Journal of Agricultural and Food Chemistry
1
1
2
Detoxification of Fusaric Acid by the Soil Microbe Mucor rouxii
3
Frankie K. Crutcher†§, Lorraine S. Puckhaber†, Alois A. Bell†, Jinggao Liu†, Sara E.
Duke†, Robert D. Stipanovic†*, and Robert L. Nichols‡
4
5
6
†USDA, Insect Control and Cotton Disease Research Unit, Southern Plains Agricultural
Research Center, Agricultural Research Service, USDA, 2765 F&B Road, College
Station, Texas 77845, USA
7
8
9
‡Cotton Incorporated, 6399 Weston Parkway, Cary, North Carolina, USA
§Current Address: Eastern Agricultural Research Center, Montana State University,
Sidney, MT 59270, USA
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
*Corresponding Author (Tel: 979 823ꢀ5670; Fax: 979 260ꢀ9319: Email: rdstip@verizon.net).
ACS Paragon Plus Environment

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
Journal of Agricultural and Food Chemistry
Page 2 of 19
2
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
ABSTRACT: Fusarium oxysporum f. sp. vasinfectum race 4 (VCG0114), which causes root rot
and wilt of cotton (Gossypium hirsutum and G. barbadense) has been identified recently for the
first time in the western hemisphere in certain fields in the San Joaquin Valley of California.
This pathotype produces copious quantities of the plant toxin fusaric acid (5ꢀbutylꢀ2ꢀ
pyridinecarboxylic acid) compared to other isolates of F. oxysporum f. sp. vasinfectum (Fov) that
are indigenous to the U. S. Fusaric acid is toxic to cotton plants and may help the pathogen
compete with other microbes in the soil. We found that a laboratory strain of the fungus Mucor
rouxii converts fusaric acid into a newly identified compound, 8ꢀhydroxyfusaric acid. The latter
compound is significantly less phytotoxic to cotton than the parent compound. Based on
bioassays of hydroxylated analogs of fusaric acid, hydroxylation of the butyl side chain of fusaric
acid may affect a general detoxification of fusaric acid. Genes that control this hydroxylation
may be useful in developing biocontrol agents to manage Fov.
KEY WORDS: Fusarium oxysporum f. sp. vasinfectum race 4 (VCG0114), cotton, Gossypium
hirsutum, Gossypium barbadense, fusaric acid, 8ꢀhydroxyfusaric acid, California Fov race 4
ACS Paragon Plus Environment

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
Page 3 of 19
Journal of Agricultural and Food Chemistry
3
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
INTRODUCTION
Fusaric acid, 1 (Figure 1) is a plant toxin that may play a role in the pathogenicity of Fusarium
oxysporum f. sp. vasinfectum (Fov) in cotton (Gossypium hirsutum, and G. barbadense).1
Recently, a Fov genotype, (CAꢀFov4), was identified for the first time in the western
hemisphere in California cotton fields,2 and it produces copious quantities of fusaric acid
compared to most Fov genotypes indigenous to the U. S.1 This pathotype causes severe yield
losses in California and is a potential risk to cotton production in other U. S. cotton growing
states. Cotton is unusually sensitive to fusaric acid compared to other plant species.3 Knockꢀout
mutants of an Australian isolate of Fov that had lost the ability to produce fusaric acid, showed
weaker pathogenicity than their wild type progenitor toward tomato (Lycopersicon esculentum)
seedlings in a seed germination bioassay on agar plates.1
Multiple analogs of fusaric acid have been shown to be less toxic to cotton cotyledons
than fusaric acid itself.4 Thus, a biocontrol agent that can detoxify fusaric acid may provide an
environmentally advantageous strategy to manage this pathogen. To this end, we have
investigated various soil microorganisms to identify those that metabolize fusaric acid. We were
particularly interested in those that survived when challenged with a relatively high dose of
fusaric acid (200 ꢀg/mL). Since we were ultimately interested in identifying a unique gene(s)
(preferably a single gene) that could be incorporated into a biocontrol agent to degrade/detoxify
fusaric, we searched for microorganisms that produced an unknown peak in the HPLC profile
that increased as the fusaric acid peak decreased. We previously reported that Aspergillus
tubengensis converts fusaric acid to fusarinol and this process is a detoxification mechanism,
but it probably involves more than one gene.5
In recent experiments, HPLC analysis of culture filtrates from Mucor rouxii and A. niger
grown in the presence of fusaric acid revealed the presence of multiple compounds including
ACS Paragon Plus Environment