Submitted to: Tree Genetics and Genomes
Publication Type: Peer reviewed journal
Publication Acceptance Date: 5/18/2012
Publication Date: 5/18/2012
Citation: Zhu, Y., Ping, Z., Vijaya, V., Dorrie, M., Curry, E.A., Mattheis, J.P. 2012. Multiple plant hormones and cell wall metabolism regulate apple fruit maturation patterns and texture attributes. Tree Genetics and Genomes. 8(6):1389-1406. Interpretive Summary: Apple is one of the most popular perennial tree fruits. Apple fruit ripening physiology and horticultural practices for better fruit quality have been extensively investigated, but little is known regarding the genetics and molecular regulation inside a ripening apple except the recent progresses on the roles of ethylene biosynthesis genes. Due to its long history and widespread cultivation, and more importantly its out-crossing nature, apple exhibits a high level of heterozygosity, great variation at ripening behaviors and quality attributes. The genetic investigations of apple fruit ripening process can hardly be represented by those on model system such as Arabidopsis, rice or popular for the anatomic feature of apple fruit and unique physiology pome fruit ripening. Understanding this molecular process is crucial for genomics-assisted apple breeding, which takes painfully long time and lots of space, due to juvenility, low heredity and large size of individual trees. Several features about this study stood out from other similar studies reported recently. 1. Parallel transcriptome profiling on two apple cultivars with distinct ripening phenotypes and texture attribute were carried out simultaneously for identifying genotype-specific transcriptome changes during ripening. 2. The customer-designed high-density apple long-oligo array included the largest collection of 23,999 available apple unigenes, to our knowledge. 3. Microscopic analysis added otherwise unavailable deep-phenotyping data; and systematic physiological data help to better align the developmental stages between two otherwise distinct cultivars. Also, RT-qPCR analysis on 12 randomly selected unigenes independently validated the array results, indicating a high quality dataset. A total of 1793 and 1209 differentially expressed unigenes, represent 7.47% and 5.04% of all unigenes deposited on the array, were identified from HC and CP, respectively. Unigenes implicated in hormone metabolism and response, cell wall biosynthesis and modification as well as those encoding transcription factors and signal transduction components were among the major transcriptomic changes during last four-week apple fruit ripening, which corresponds to dramatic transformation in fruit texture. The results from this study added significant contribution in deciphering the molecular mechanisms regulating apple fruit ripening and quality. Plant hormone function and cell wall metabolism might be the “usual suspects” for ripening regulation, yet most of the identified unigenes and associated pathways have never been previously reported. This is a carefully-designed and well-analyzed large-scale whole transcriptome analysis focusing on cultivar-specific apple ripening regulation; moreover, most of the identified unigenes can be further studied in an available population crossed between these two cultivars, as well as other germplasm, for their general association with specific phenotype, such as ripening date (season), fruit firmness and crispness.
Technical Abstract: Molecular events regulating apple fruit ripening and sensory quality are largely unknown. Such knowledge is essential for genomic-assisted apple breeding and postharvest quality management. In this study, a parallel transcriptome profile analysis, scanning electron microscopic (SEM) examination and systematic physiological characterization were performed on two apple cultivars, Honeycrisp (HC) and Cripps Pink (CP), which have distinct ripening features and texture attributes. Systematic physiological characterization of fruit ripening based on weekly maturity data indicated substantial differences of fruit crispness and firmness at comparable ripening stages. SEM images of fruit cortex tissues prepared from fruits with equivalent maturity suggested that the cell wall thickness may contribute to the observed phenotypes of fruit firmness and crispness. A high-density long-oligo apple microarray consisting of duplex 190,135 cross-hybridization-free 50-70-mer isothermal probes, and representing 23,997 unigenes was manufactured on a Nimblegen array platform. Transcriptome profiling identified a total of 1793 and 1209 unigenes differentially expressed during ripening from cortex tissues of HC and CP, respectively. Unigenes implicated in hormone metabolism and response, cell wall biosynthesis and modification and those encoding transcription factors were among the prominent functional groups. Between two cultivars, most of the identified unigenes were similarly regulated during fruit ripening, however, a short list of gene families or specific family members exhibited distinct expression patterns between the two cultivars, which may represent candidate genes regulating cultivar-specific apple fruit ripening patterns and quality attributes.