Genotype- and tissue-specific metabolic networks and hub genes involved in water-induced distinct sweet cherry fruit cracking phenotypes

Michail Michailidis; Evangelos Karagiannis; Christos Bazakos; Georgia Tanou; Ioannis Ganopoulos; Athanassios Molassiotis

doi:10.1016/j.csbj.2021.09.030

Genotype- and tissue-specific metabolic networks and hub genes involved in water-induced distinct sweet cherry fruit cracking phenotypes

Comput Struct Biotechnol J. 2021 Sep 28:19:5406-5420. doi: 10.1016/j.csbj.2021.09.030. eCollection 2021.

Authors

Michail Michailidis¹, Evangelos Karagiannis¹, Christos Bazakos^{2

3

4}, Georgia Tanou^{3

5}, Ioannis Ganopoulos^{2

3}, Athanassios Molassiotis¹

Affiliations

¹ Laboratory of Pomology, Department of Horticulture, Aristotle University of Thessaloniki, Thessaloniki-Thermi 57001, Greece.
² Institute of Plant Breeding and Genetic Resources, ELGO-DEMETER, Thessaloniki , Greece.
³ Joint Laboratory of Horticulture, ELGO-DEMETER, Thessaloniki-Thermi 57001, Greece.
⁴ Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linne-Weg 10, Cologne 50829, Germany.
⁵ Institute of Soil and Water Resources, ELGO-DEMETER, Thessaloniki-Thermi 57001, Greece.

Abstract

Sweet cherry fruit cracking is a complex physiological disorder that causes significant economic losses. Despite many years of research there is a lack of understanding of the mechanisms involved in cracking. Here, skin and flesh tissue from the cracking susceptible 'Early Bigi' and the cracking tolerant 'Regina' cultivars were sampled prior and just after water dipping treatment to identify water-affected metabolic networks that putatively involved in fruit cracking. Primary metabolites, most strongly those involved in sugars and amino acid metabolism, such as glucose and asparagine, shifted in 'Early Bigi' compared with 'Regina' tissues following water exposure. Comparisons between cultivars, tissues and dipping points identified significant differentially expressed genes. Particularly, genes related to abscisic acid, ethylene biosynthesis, pectin metabolism, expansins and aquaporins were altered in water-exposed tissues. To further characterize the role of these genes in cracking, their single nucleotide variants of the coding regions was studied in another eight sweet cherry cultivars, which differ in their sensitivity to cracking, revealing a strong link mainly between pectin metabolism-related genes and cracking-phenotypes. Integrated metabolomic and transcriptomic profiling uncovered genotypic- and tissue-specific metabolic pathways, including tricarboxylic acid cycle, cell enlargement, lipid and ethanol biosynthesis, and plant defense that putatively are involved in fruit cracking. Based on these results, a model which describes the skin and flesh metabolic reprogramming during water-induced fruit cracking in the susceptible 'Early Bigi' cultivar is presented. Τhis study can help to explore novel candidate genes and metabolic pathways for cracking tolerance in sweet cherry.

Keywords: Abscisic acid; Ethylene; Expansins; Flesh and skin tissues; Fruit cracking; Metabolomic; Pectin; Sweet cherry; Transcriptomic; Water dipping.