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Thousand Cankers Disease of Eastern Black Walnut: Ecological Interactions in the Holobiont of a Bark Beetle-Fungal Disease

<p>Eastern black walnut (<i>Juglans
nigra</i> L.) ranks among the most highly valued timber species in the central
hardwood forest and across the world. This valuable tree fills a critical role
in native ecosystems as a mast bearing pioneer on mesic sites. Along with other
<i>Juglans</i> spp. (Juglandaceae), <i>J. nigra</i> is threatened by thousand
cankers disease (TCD), an insect-vectored disease first described in 2009. TCD
is caused by the bark beetle <i>Pityophthorus
juglandis</i> Blackman (Corthylini) and the phytopathogenic fungus <i>Geosmithia morbida</i> Kol. Free. Ut. &
Tiss. (Bionectriaceae). Together, the <i>P.
juglandis</i>-<i>G. morbida</i> complex has
expanded from its historical range in southwest North America throughout the
western United States (U.S.) and Europe. This range expansion has led to
widespread mortality among naïve hosts <i>J.
nigra</i> and <i>J. regia</i> planted
outside their native distributions.</p>

<p> The severity
of TCD was previously observed to be highest in urban and plantation
environments and outside of the host native range. Therefore, the objective of
this work was to provide information on biotic and abiotic environmental
factors that influence the severity and impact of TCD across the native and
non-native range of <i>J. nigra</i> and
across different climatic and management regimes. This knowledge would enable a
better assessment of the risk posed by TCD and a basis for developing
management activities that impart resilience to natural systems. Through a
series of greenhouse-, laboratory- and field-based experiments, environmental
factors that affect the pathogenicity and/or survival of <i>G. morbida</i> in <i>J. nigra</i>
were identified, with a focus on the microbiome, climate, and opportunistic
pathogens. A number of potentially important interactions among host, vector,
pathogen and the rest of the holobiont of TCD were characterized. The <i>holobiont</i> is defined as the whole
multitrophic community of organisms—including <i>J. nigra</i>, microinvertebrates, fungi and bacteria—that interact with
one another and with the host.</p>

<p>Our findings indicate that
interactions among host, vector, pathogen, secondary pathogens, novel microbial
communities, and novel abiotic environments modulate the severity of TCD in
native, non-native, and managed and unmanaged contexts. Prevailing climatic
conditions favor reproduction and spread of <i>G.
morbida</i> in the western United States due to the effect of wood moisture
content on fungal competition. The microbiome of soils, roots, and stems of
trees and seedlings grown outside the host native range harbor distinct,
lower-diversity communities of bacteria and fungi compared to the native range,
including different communities of beneficial or pathogenic functional groups
of fungi. The pathogen <i>G. morbida</i> was
also associated with a distinct community of microbes in stems compared to <i>G. morbida</i>-negative trees. The soil
microbiome from intensively-managed plantations facilitated positive feedback
between <i>G. morbida</i> and a
disease-promomting endophytic <i>Fusarium
solani</i> species complex sp. in roots of <i>J.
nigra</i> seedlings. Finally, the nematode species <i>Bursaphelenchus juglandis</i> associated with <i>P. juglandis</i> synergizes with <i>G.
morbida</i> to cause foliar symptoms in seedlings in a shadehouse; conversely,
experiments and observations indicated that the nematode species <i>Panagrolaimus</i> sp. and cf. <i>Ektaphelenchus</i> sp. could suppress WTB
populations and/or TCD outbreaks.</p>

<p>In conclusion, the composition,
function, and interactions within the <i>P.
juglandis</i> and <i>J. nigra</i> holobiont play
important roles in the TCD pathosystem. Managers and conservationists should be
aware that novel associations outside the host native range, or in monocultures,
intensive nursery production, and urban and low-humidity environments may favor
progression of the disease through the effects of associated phytobiomes,
nematodes, and climatic conditions on disease etiology. Trees in higher
diversity, less intensively managed growing environments within their native
range may be more resilient to disease. Moreover, expatriated, susceptible host
species (<i>i.e.</i>, <i>J. nigra</i>) growing in environments that are favorable to novel pests
or pest complexes (<i>i.e.</i>, the western
U.S.) may provide connectivity between emergent forest health threats (<i>i.e.</i>, TCD) and native host populations (<i>i.e.</i>, <i>J. nigra</i> in its native range).</p>

  1. 10.25394/pgs.15057828.v1
Identiferoai:union.ndltd.org:purdue.edu/oai:figshare.com:article/15057828
Date27 July 2021
CreatorsGeoffrey M Williams (11186766)
Source SetsPurdue University
Detected LanguageEnglish
TypeText, Thesis
RightsCC BY 4.0
Relationhttps://figshare.com/articles/thesis/Thousand_Cankers_Disease_of_Eastern_Black_Walnut_Ecological_Interactions_in_the_Holobiont_of_a_Bark_Beetle-Fungal_Disease/15057828

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