Morphological variants of Moniliophthora roreri on artificial media and the biotroph/necrotroph shift

Authors: Bailey, Bryan; ALI, SHAHIN - Non ARS Employee; Strem, Mary; Meinhardt, Lyndel

Submitted to: Fungal Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/12/2018
Publication Date: 7/1/2018
Citation: Bailey, B.A., Ali, S., Strem, M.D., Meinhardt, L.W. 2018. Morphological variants of Moniliophthora roreri on artificial media and the biotroph/necrotroph shift. Fungal Biology. 122(7):701-716.

Interpretive Summary: Moniliophthora roreri causes frosty pod rot of cacao, a disease which destroys cacao yields throughout production areas in the western hemisphere. Moniliophthora perniciosa, causes witches’ broom disease and is similarly destructive to cacao yields throughout many of the same areas where M. roreri occurs. The use of molecular tools has made clear the close genetic relationships between the two species which are commonly considered sister species. By understanding the differences and similarities between their biology and genetic diversity we hope to manage the diseases they cause. This includes the use to disease tolerant cacao. Here we compare what is known about M. roreri and M. perniciosa, and the diseases they cause focusing on their interactions with cacao. We present, for the first time, a comprehensive evaluation of M. roreri’s complex life cycle, documenting the parasitic (biotrophic) and saprophytic (necrotropic) phases in culture. We also present and make direct comparisons between the patterns of M. roreri genes expressed throughout the infection process on tolerant and susceptible cacao. This study answers questions concerning the biology of M. roreri identifying weaknesses in the pathogen that can be exploited in its field management, including the use of disease tolerant cacao. These results will be used by scientists seeking to develop better disease management practices including the optimized use of disease tolerant germplasm. Ultimately this research benefits cacao growers, the chocolate industry, and consumers by stabilizing cacao yields and commodity supplies.

Technical Abstract: Moniliophthora roreri is an unusual fungus and plant pathogen on many levels. Although M. roreri is an aggressive pathogen of cacao (Theobroma cacao), many species grouped in the genus Moniliophthora are considered endophytes. The morphology of M. roreri is confusing and for many years it was considered an ascomycete, although we now know it to be a basidiomycete. M. roreri, as it turns out, shares a close genetic relationship with another pathogen of cacao. Moniliophthora perniciosa causes witches’ broom disease, a devastating disease of cacao in its own right. M. perniciosa has a more typical basidiomycete lifestyle, forming clamp connections in its dikaryotic phase and producing basidiospore-forming mushrooms. Basidiospores are the infective units spreading the disease through infections of meristematic tissues including flower cushions, stem tips, and pods. In contrast, M. roreri does not form clamp connections or mushrooms, only infects pods, and the derivation of its infective spores is a point of contention. Both pathogens are hemibiotrophs having prolonged biotrophic phases followed by distinctly different necrotrophic phases. Both pathogens are limited to the Western hemisphere but their potential threat to cacao producing regions around the world is obvious. Fortunately, our knowledge concerning both M. roreri and M. perniciosa has expanded in recent years with the exploitation of molecular technologies. Draft genomes of both species have been published and the genetic diversity and distribution of both pathogens is better understood. Together, these two pathogens form a dynamic double threat to cacao production. A detailed histological evaluation of the in vitro germination of M. roreri spores and development of biotrophic/necrotrophic mycelia is provided. In addition, the direct comparison of previously described transcriptome data derived under diverse experimental conditions strengthens our current understanding of the M. roreri/cacao interaction. Understanding the biology and potential for adaptation of these pathogens is critical for proper evaluation and deployment of resistance/tolerance resources now and will be into the future. In this manuscript the discussion will focus on the molecular biology of M. roreri although comparisons will be made to M. perniciosa throughout.