Elucidating the molecular responses of apple rootstock resistant to ARD pathogens: Challenges and opportunities for development of genomics-assisted breeding tools

Authors: Zhu, Yanmin; Fazio, Gennaro; Mazzola, Mark

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/8/2014
Publication Date: 8/20/2014
Citation: Zhu, Y., Fazio, G., Mazzola, M. 2014. Elucidating the molecular responses of apple rootstock resistant to ARD pathogens: Challenges and opportunities for development of genomics-assisted breeding tools. Horticulture Research. https://doi.org/10.1038/hortres.2014.43.
DOI: https://doi.org/10.1038/hortres.2014.43

Interpretive Summary: Apple Replant Disease (ARD) is one of the major limitations to the establishment of an economically viable orchard on replant sites due to the buildup and long-term survival of pathogen inoculum. Utilizing resistant rootstocks as an integral component for replant disease management are crucial to the sustainability and profitability. Nevertheless, the mechanism and resources of resistance to soilborne pathogens is poorly characterized, largely due to the lack of reliable phenotyping methods for resistance traits and the hidden nature of root systems. Identification of the molecular genetics controlling the defense mechanisms to soilborne necrotrophic pathogens is an essential step. Further developing molecular tools or biomarkers for genomics-assisted breeding will facilitate the incorporation of resistant traits to new apple rootstock varieties more efficiently and accurately. So far, majority of the investigations regarding plant defense responses to necrotrophic foliar pathogens are from foliar pathogens and on Arabidopsis and other model species; the transferability of these knowledge to root tissues of perennial tree crop is unknown. This review aims to summarize the current understanding of the molecular framework underlying plant and pathogen interaction. Plant defense responses consist of several interacting modules and operate as a network. Upon pathogen detection by plants, cellular signals such as oscillation of Ca2+ concentration, reactive oxygen species (ROS) burst and protein kinase activity, lead to plant hormone biosynthesis and signaling. The hormones jasmonic acid (JA) and ethylene (ET) are central to the induction and regulation of defense mechanisms toward invading necrotrophic pathogens. Complicated hormone crosstalk modulates the fine-tuning of transcriptional reprogramming and metabolic redirection, resulting in production of antimicrobial metabolites, cell wall refortification, and enzyme inhibitors to restrict pathogen progression. Our recent RNA-Seq based transcriptome analysis on defense responses in apple roots to Pythium ultimum infection suggest the conserved features of resistant mechanisms in perennial root system to those operating in foliar tissues of model plant systems. It is conceivable that the timing and intensity of genotype-specific defense responses may lead to different outcomes toward invading necrotrophic pathogens. Further research on apple root resistant responses should assist developing molecular tools or biomarkers for targeted incorporation resistance traits into future apple rootstock varieties.

Technical Abstract: Apple Replant Disease (ARD) is one of the major limitations to the establishment of an economically viable orchard on replant sites due to the buildup and long-term survival of pathogen inoculum. Infection by several soilborne necrotrophic fungi and oomycetes is primarily responsible for ARD and results in symptoms ranging from serious growth inhibition to death of young trees. Chemical fumigation has been the conventional method used for control of ARD and manipulating soil microbial ecology has been explored to reduce pathogen density and aggressiveness. To date, innate resistance of apple rootstock has not been carefully explored as a means to control this disease, partly due to its complex etiology and difficulty in phenotyping the disease resistant trait. Defense responses in plant roots to soilborne necrotrophic pathogens are poorly characterized, but considerable progress has been achieved using foliar disease systems. Plant defense responses consist of several interacting modules and operate as a network. Upon pathogen detection by plants, cellular signals such as oscillation of Ca2+ concentration, reactive oxygen species (ROS) burst and protein kinase activity, lead to plant hormone biosynthesis and signaling. The hormones jasmonic acid (JA) and ethylene (ET) are central to the induction and regulation of defense mechanisms toward invading necrotrophic pathogens. Complicated hormone crosstalk modulates the fine-tuning of transcriptional reprogramming and metabolic redirection, resulting in production of antimicrobial metabolites, cell wall refortification, and enzyme inhibitors to restrict pathogen progression. The recent transcriptome profiling of apple rootstocks in response to inoculation with the ARD pathogen Pythium ultimum demonstrated that there is a high-degree of conservation with foliar tissues regarding the molecular framework of defense responses to pathogen challenge. It is conceivable that the timing and intensity of genotype-specific defense responses may lead to different outcomes in defending against the invading necrotrophic pathogens. Elucidation of host defense mechanisms is critical in developing molecular tools for genomics-assisted breeding of resistant apple rootstocks. Due to its perennial nature, use of resistant rootstocks as a component for disease management might offer a higher level and longer-term benefit to tree performance than the standard practice of soil fumigation for control of ARD.