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Extensive transcriptomic studies on the roles played by abscisic acid and auxins in the development and ripening of strawberry fruits

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Abstract

Strawberry is an ideal model for studying the molecular biology of the development and ripening of non-climacteric fruits. Hormonal regulation of gene expression along all these processes in strawberries is still to be fully elucidated. Although auxins and ABA have been pointed out as the major regulatory hormones, few high-throughput analyses have been carried out to date. The role for ethylene and gibberellins as regulatory hormones during the development and ripening of the strawberry fruit remain still elusive. By using a custom-made and high-quality oligo microarray platform done with over 32,000 probes including all of the genes actually described in the strawberry genome, we have analysed the expression of genes during the development and ripening in the receptacles of these fruits. We classify these genes into two major groups depending upon their temporal and developmental expression. First group are genes induced during the initial development stages. The second group encompasses genes induced during the final maturation and ripening processes. Each of these two groups has been also divided into four sub-groups according their pattern of hormonal regulation. By analyzing gene expression, we clearly show that auxins and ABA are the main and key hormones that combined or independently are responsible of the development and ripening process. Auxins are responsible for the receptacle fruit development and, at the same time¸ prevent ripening by repressing crucial genes. ABA regulates the expression of the vast majority of genes involved in the ripening. The main genes expressed under the control of these hormones are presented and their physiological rule discussed. We also conclude that ethylene and gibberellins do not seem to play a prominent role during these processes.

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Abbreviations

ABA:

Abscisic acid

Ct :

Threshold cycle

EST:

Expressed sequence tag

G1:

Green1 development stage

G3:

Green3 development stage

GAs:

Gibberellins

GO:

Gene ontology

IAA:

Indole-3-acetic acid

MEP:

2-C-methyl-d-erithritol 4-phosphate pathway

MVA:

Mevalonate pathway

NCED:

9-cis-Epoxycarotenoid dioxygenase

NDGA:

Nordihydroguaiaretic acid

qRT-PCR:

Quantitative real-time-polymerase chain reaction

R:

Red ripe ripening stage

TFs:

Transcription factors

Tm:

Melting temperature

u.a.i:

Arbitrary units of intensity

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Acknowledgments

This work was supported by a grant from the Ministerio Español de Ciencia e Innovación (MICINN) (BIO2010-19322). LMP and RBP are grateful for the award of a Ph.D. fellowship within the framework of Formación del Personal Universitario (FPU) program implemented by the Ministerio de Educación y Ciencia (MEC) (Spain) and a post-doctoral contract from Campus de Excelencia Internacional Agroalimentario (CEIA3) from University of Córdoba, respectively.

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    Authors and Affiliations

    1. Departamento de Bioquímica y Biología Molecular. Edificio Severo Ochoa, Campus Universitario de Rabanales y Campus de Excelencia Internacional Agroalimentario CEIA3, Universidad de Córdoba, 14071, Córdoba, Spain

      Laura Medina-Puche, Rosario Blanco-Portales, Francisco Javier Molina-Hidalgo, Guadalupe Cumplido-Laso, Nicolás García-Caparrós, Enriqueta Moyano-Cañete, José Luis Caballero-Repullo, Juan Muñoz-Blanco & Antonio Rodríguez-Franco

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    1. Laura Medina-Puche
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    3. Francisco Javier Molina-Hidalgo
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    4. Guadalupe Cumplido-Laso
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    5. Nicolás García-Caparrós
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    7. José Luis Caballero-Repullo
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    8. Juan Muñoz-Blanco
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    9. Antonio Rodríguez-Franco
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    Corresponding author

    Correspondence to Juan Muñoz-Blanco.

    Additional information

    Laura Medina-Puche and Rosario Blanco-Portales contributed equally to this work.

    Additional files

    Below is the link to the electronic supplementary material.

    ESM 1

    Table S1. List of primer sequences used for validation through qRT-PCR. Fw: forward; Rv: reverse. (DOCX 26 kb)

    ESM 2

    Table S2. Gene expression values of different housekeeping genes obtained by qRT-PCR analysis. Experiment A: throughout the development and ripening of strawberry fruit. Experiment B: in vegetative tissues against strawberry red fruit. Experiment C: in de-achened G2 fruits against control G2 fruits. Reactions normalized using the Ct value corresponding to a strawberry interspacer 26S-18S gene for quantification as described in Materials and Methods. Ct values used as reference were assigned an arbitrary value equal to unity. The increase in mRNA value was relative to the receptacle G1-Ct value for experiment A, to the receptacle R-Ct value for experiment B and to the control G2-fruits-Ct for experiment C. G1: small-sized green fruits; G2: middle-sized green fruits; G3: full-sized green fruits; W: white fruits; R: full-ripe red fruits. (XLSX 11 kb)

    ESM 3

    Table S3. Complete list of genes expressed during fruit ripening. Data provided correspond to strawberry genes whose expression change from green inmature to red ripe fruit receptacles. Gene ID as reported in Fragaria vesca Genome Database (http://www.strawberrygenome.org/). (XLSX 1808 kb)

    ESM 4

    Table S4. List of genes deregulated after ABA depletion by using NDGA. List of strawberry genes whose expression is modified after NDGA treatment respect to untreated control fruits. Gene ID reported in Fragaria vesca Genome Database (http://www.strawberrygenome.org/). (XLSX 1157 kb)

    ESM 5

    Table S5. Complete list of differential gene expression in red ripe strawberry fruit receptacles compared to vegetative tissues. Gene ID reported in Fragaria vesca Genome Database (http://www.strawberrygenome.org/). (XLSX 1218 kb)

    ESM 6

    Table S6. Correlation coefficients (r-value) and coefficients of determination (r-squared) calculated with data obtained from each of the three biological replicates under the experimental conditions summarized in Fig. 1. This was calculated by fitting the normalized data to a linear mode using the lm() R function. (DOCX 13 kb)

    ESM 7

    Table S7. Validation of microarray data by qRT-PCR. (XLSX 15 kb)

    ESM 8

    Tables S8-S15. GO annotation of differentially regulated genes in Clusters UP and DOWN regulated. (XLSX 341 kb)

    ESM 9

    Tables S16-S25. Annotation of differentially regulated genes in each functional group sorted into the four ripening Up-regulated clusters. Transcriptomic analyses of genes whose expression changes during fruit ripening, in fruits treated with NDGA, in de-achened fruits and specificity in receptacle. NDGA and minus achenes indicate the expression obtained for the genes studied in green–white fruits injected with NDGA 100 μm and green2 fruits whose achenes were removed, respectively. Intensity (a.u.i.) indicates the total signal intensity for each feature on the microarray platform. Gene ID as reported in Fragaria vesca Genome Database (http://www.strawberrygenome.org/). (XLSX 1135 kb)

    ESM 10

    Tables S26-S29. Annotation of differentially down regulated genes sorted into functional groups. Transcriptomic analyses of genes whose expression changes during fruit ripening, in fruits treated with NDGA, in de-achened fruits and specificity in receptacle. NDGA and minus achenes indicate the expression obtained for the genes studied in green–white fruits injected with NDGA 100 μm and green2 fruits whose achenes were removed, respectively. Intensity (a.u.i.) indicates the total signal intensity for each feature on the microarray platform. Gene ID as reported in Fragaria vesca Genome Database (http://www.strawberrygenome.org/) (XLSX 123 kb)

    ESM 11

    Fig. S1. Distribution of the differentially expressed genes according their gene onthologies functional terms (GO terms) for categories Biological Process, Molecular Function and Cellular Component. (PDF 796 kb)

    ESM 12

    File S1. Supplemental references cited in Tables 2, 3, 4, 5, 6, 7, 8, 9 and 10 and Tables S16–S29. (XLSX 123 kb)

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    Medina-Puche, L., Blanco-Portales, R., Molina-Hidalgo, F.J. et al. Extensive transcriptomic studies on the roles played by abscisic acid and auxins in the development and ripening of strawberry fruits. Funct Integr Genomics 16, 671–692 (2016). https://doi.org/10.1007/s10142-016-0510-3

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