Molecular and metabolic changes of cherelle wilt of cacao and its effect on Moniliophthora roreri

Authors: Melnick, Rachel; Strem, Mary; CROZIER, JAYNE - Catie Tropical Agricultural Research; Sicher Jr, Richard; Bailey, Bryan

Submitted to: Physiological and Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/30/2013
Publication Date: 10/1/2013
Citation: Melnick, R.L., Strem, M.D., Crozier, J., Sicher, Jr., R.C., Bailey, B.A. 2013. Molecular and metabolic changes of cherelle wilt of cacao and its effect on Moniliophthora roreri. Physiological and Molecular Plant Pathology. 84:153-162.

Interpretive Summary: The tree Theobroma cacao (cacao) is the source of chocolate. Cherelle wilt, a natural process, results in the loss of large numbers of young cacao pods (cherelles) by their premature death. Frosty pod disease caused by the fungus Moniliophthora roreri, also causes large yield losses for cacao. Cherelles that are wilting can also be infected with Moniliophthora roreri. We used molecular techniques to characterize changes in pod biological processes associated with death of young pods due to cherelle wilt. We also used these techniques to determine how cherelle wilt influences frosty pod disease development. Cherelle wilt blocks the normal frosty pod disease process preventing the fungus from reproducing. Therefore, wilting pods infected with Moniliophthora roreri do not contribute to the disease cycle. This research could benefit cacao farmers throughout the world by leading to new methods for limiting pod loss due to cherelle wilt and providing new ideas on how to block the frosty pod disease process. In addition, this information provides farmers with the knowledge that removal of wilted cherelles from fields is not necessary to reduce frosty pod disease spread.

Technical Abstract: The seeds of Theobroma cacao L. pods are processed into cocoa products. Cherelle wilt is physiological thinning of young pods that result in loss of potential pods. Cherelle wilt first occurs 50 days after pollination (DAP) and a second thinning occurs around 70 DAP. Cherelles are also highly susceptible to infection by the fungus Moniliophthora roreri (Mr), causal agent of frosty pod rot (FPR). The goals of this research were to increase our understanding of the cherelle wilt process and its impact on Mr infection using the methods of microscopic, metabolite, and gene expression analysis. Wilting was associated with increased levels of TCA cycle intermediaries (glyceric, fumaric and succinic acids) and decreased levels of key transport compounds (myo-inositol, sucrose). Changes in the expression of cacao ESTs in response to cherelle wilt suggests induction of the polyamine, ethylene, and jasmonic acid biosynthetic pathways and changes in expression patterns for cacao ESTs regulating auxin and cytokinin levels. The presence of thick fungal mycelia was considered indicative of Mr infection in malformed green and malformed yellow (wilting) cherelles and profuse thin mycelia was observed in wilting cherelles after they browned. Although often causing pod malformation, infection by Mr otherwise caused little alteration of cherelle physiology during the early stages of FPR. A lack of altered Mr gene expression during the early stages of wilt (yellow cherelles) indicated that the Mr response to senescence associated with wilt was delayed. As wilt progressed and cherelles browned without observed Mr sporulation, Mr responded to the unfavorable environment by altering the expression of ESTs associated with metabolite detoxification and host tissue degradation. The observed physiological changes associated with cherelle wilt are common with senescencing fruit and provide an antagonistic environment which appears to disrupt the Mr lifecycle, possibly explaining the lack of Mr sporulation on infected cherelles undergoing wilt.