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Multiple plant hormones and cell wall metabolism regulate apple fruit maturation patterns and texture attributes

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Abstract

Global transcriptional regulation during apple fruit maturation and associated texture changes were assessed by transcriptome profiling and systematic characterization of maturation progression of two cultivars, ‘Honeycrisp’ (HC) and ‘Cripps Pink’ (CP). A high-density long-oligo apple microarray consisting of duplex 190,135 cross-hybridization-free 50–70-mer isothermal probes, representing 23,997 unigenes, was designed for and manufactured on a NimbleGen array platform. Cortex tissues from both HC and CP at three maturation stages, i.e., 4, 2, and 0 week(s) before physiological maturity, were utilized for transcriptome profiling. A total of 1,793 and 1,209 differentially expressed unigenes, 7.47 % and 5.04 % of all unigenes deposited on the array, were identified from HC and CP, respectively. Unigenes associated with ethylene biosynthesis and response, auxin homeostasis and transport, gibberellin reception and metabolism as well as degradation of hemicelluloses may contribute to the observed phenotypic variations in apple maturation patterns and texture attributes such as fruit firmness and crispness. Microarray data validation indicated that more than 85 % of randomly selected unigenes showed consistent expression patterns with qRT-PCR results. Physiological characterization demonstrated substantial differences in maturation progression between these two cultivars, and a remarkable transformation in fruit texture occurred from week −4 to week 0.

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Acknowledgments

The authors are grateful to Ann Callahan, Chris Dardick, Cindy Tong, and Tianbao Yang for their helpful comments. The authors wish to thank Xia Rui for preparation of Table S1 and Table S2. We wish to thank Mallela Magana, Janie Countryman, Edward Valdez, and Bruce Mackey for their contribution in fruit harvest, maturity test, tissue collection, and other excellent technical assistance. This study was supported by Washington Tree Fruit Research Commission and USDA base fund.

The authors declare that the experiments comply with the current laws of USA. All authors read and approved the final manuscript, and declared no conflict of interest.

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Authors and Affiliations

  1. Agriculture Research Service, Tree Fruit Research Laboratory, United States Department of Agriculture, 1104 N. Western Ave., Wenatchee, WA, 98801, USA

    Yanmin Zhu, Sungbong Shin, Eric Curry & James P. Mattheis

  2. Department of Horticulture and Landscape Architecture, Washington State University, 151 Johnson Hall, Pullman, WA, 99164-6414, USA

    Ping Zheng, Vijaya Varanasi & Dorrie Main

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  1. Yanmin Zhu
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Correspondence to Yanmin Zhu.

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Communicated by A. Dandekar

Yanmin Zhu and Ping Zheng contributed equally to this work.

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Fig. S1

Overall distribution of identified unigenes in major functional categories. a Distribution of different expression patterns among identified unigenes. Column with green color represented those identified from HC, and column with pink color was from CP. Values of Y-axis indicated the numbers of unigenes. X-axis indicates four different expression patterns for both cultivars. Refer to Tables 3, 4, and S1, S2, S3 and S4 for detailed information of individual unigenes. b Cultivar specificity of identified unigenes implicated in plant hormone metabolism and responses. c Cultivar specificity of unigenes implicated in cell wall metabolisms. d Cultivar specificity of TF-encoding unigenes. In (b), (c), and (d), Y-axis showed the numbers of up- or down-regulated values (all unigenes have two values of fold change). Column with blue color represented those identified with up-regulated expression pattern, and column with red color represented those identified with down-regulated expression pattern (JPEG 105 kb)

High resolution image (TIFF 309 kb)

Fig. S2

Cultivar-specific expression patterns for unigenes in plant hormone functions. a Unigenes implicated in ethylene metabolism and response. b Unigenes implicated in auxin metabolism, transport, and response. c Unigenes implicated in GA metabolism and response. d Unigenes implicated in the metabolism and response of other plant hormones. Y-axis showed the up- or down-regulated values of identified unigenes (all unigenes have two values of fold changes). Column with blue color represented those identified with up-regulated expression pattern, and column with red color represented those identified with up-regulated expression pattern (JPEG 90 kb)

High resolution image (TIFF 261 kb)

Fig. S3

Cultivar-specific expression patterns for unigenes in carbohydrate metabolism and cell wall modification. a Unigenes encoding glycosyl transferase (GT). b Unigenes encoding glycosyl hydrolase (GH). c Unigenes encoding polysaccharide lyase and carbohydrate esterase. d Unigenes encoding expansin and other cell wall proteins. Y-axis showed the number of either up- or down-regulated values (all unigenes have two values of fold changes). Column with blue color represented those identified with up-regulated expression pattern, and column with red color represented those identified with up-regulated expression pattern (JPEG 93 kb)

High resolution image (TIFF 260 kb)

Fig. S4

Cultivar-specific expression patterns of unigenes encoding TFs. a Unigenes encoding transcription factors which specifically respond to ethylene. b Unigenes encoding transcription factors which specifically respond to auxin. c Unigenes encoding transcription factors belong to other TF families. Y-axis showed the number of either up- or down-regulated value (all unigenes have two values of fold changes). In (b) and (c), column with blue color represented those identified with up-regulated expression pattern, and column with red color represented those identified with up-regulated expression pattern (JPEG 90 kb)

High resolution image (TIFF 206 kb)

Fig. S5

Relative expression level of randomly selected unigenes by qRT-PCR. Bars represent normalized values of qRT-PCR assay; two independent RNA samples were used in separated cDNA synthesis and PCR reactions were repeated twice in triplicates for each cDNA. Y-axis indicated the relative gene expression, and X-axis showed samples at different maturation stages. Names of the selected unigenes were placed at the top of each square. Values at the bottom of each square were the fold changes based from microarray dataset one for between week −4 and week −2 and another for week −2 to week 0. Numbers highlighted in red color represented the consistent gene expression patterns between microarray analysis and qRT-PCR assay, while those highlighted in blue color represented inconsistent patterns between two methods. HC ‘Honeycrisp’, CP ‘Cripps Pink’ (JPEG 896 kb)

High resolution image (TIFF 1512 kb)

Table S1

Visual representation of differentially expressed unigenes with the annotated function in plant hormone metabolism and responses (DOC 503 kb)

Table S2

Visual representation of differentially expressed unigenes with the annotated function in cell wall metabolism and modification (DOC 604 kb)

Table S3

Differentially expressed transcription factor encoding unigenes (DOC 280 kb)

Table S4

Differentially expressed unigenes with other annotated molecular functions (XLS 70 kb)

Table S5

Primer sequences used for data validation by qRT-PCR (DOC 33 kb)

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Zhu, Y., Zheng, P., Varanasi, V. et al. Multiple plant hormones and cell wall metabolism regulate apple fruit maturation patterns and texture attributes. Tree Genetics & Genomes 8, 1389–1406 (2012). https://doi.org/10.1007/s11295-012-0526-3

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