Deciphering the Molecular Signatures Associated With Resistance to Botrytis cinerea in Strawberry Flower by Comparative and Dynamic Transcriptome Analysis

Abstract

Gray mold caused by Botrytis cinerea, which is considered to be the second most destructive necrotrophic fungus, leads to major economic losses in strawberry (Fragaria × ananassa) production. B. cinerea preferentially infects strawberry flowers and fruits, leading to flower blight and fruit rot. Compared with those of the fruit, the mechanisms of flower defense against B. cinerea remain largely unexplored. Therefore, in this study, we aimed to unveil the resistance mechanisms of strawberry flower through dynamic and comparative transcriptome analysis with resistant and susceptible strawberry cultivars. Our experimental data suggest that resistance to B. cinerea in the strawberry flower is probably regulated at the transcriptome level during the early stages of infection and strawberry flower has highly complex and dynamic regulatory networks controlling a multi-layered defense response to B. cinerea. First of all, the higher expression of disease-resistance genes but lower expression of cell wall degrading enzymes and peroxidases leads to higher resistance to B. cinerea in the resistant cultivar. Interestingly, CPKs, RBOHDs, CNGCs, and CMLs comprised a calcium signaling pathway especially play a crucial role in enhancing resistance by increasing their expression. Besides, six types of phytohormones forming a complex regulatory network mediated flower resistance, especially JA and auxin. Finally, the genes involved in the phenylpropanoid and amino acids biosynthesis pathways were gene sets specially expressed or different expression genes, both of them contribute to the flower resistance to B. cinerea. These data provide the foundation for a better understanding of strawberry gray mold, along with detailed genetic information and resistant materials to enable genetic improvement of strawberry plant resistance to gray mold.

Comparative transcriptome profiling and co-expression network analysis uncover the key genes associated with pear petal defense responses against Monilinia laxa infection

“…At the same time, it is also the initial target for M. laxa during penetration as its disassembly contributes to susceptibility to pathogen invasion ( Garcia-Benitez et al., 2019 ; Haile et al., 2019 ). Particularly, in the Kristalli cultivar, many DEGs involved in cell wall modification were differentially regulated at 2 HAI, as already described in strawberries upon Botrytis infection ( Haile et al., 2019 ; Xiao et al., 2022 ). Thus, the constitutive upregulation of DEGs associated with hampering pathogen penetration, including CCR genes, along with the simultaneous suppression of PG genes, strongly mitigated the effect of susceptibility during M. laxa infection, as was also reported during B. cinerea infection in kiwi fruits ( Cantu et al., 2008 ; Zambounis et al., 2020 ).…”

“…Despite the considerable losses due to blossom blight caused by M. laxa , the molecular interplay between this necrotrophic fungus and pear petals has not yet been deciphered. Previously, it was recorded that 19, 35, and 7 WRKY-encoding genes were involved in the regulation of defense responses in rose petals, grapevine, and strawberry flowers to Botrytis cinerea , respectively ( Haile et al., 2017 ; Liu et al., 2018 ; Xiao et al., 2022 ). TFs are key regulators of the host transcriptional reprogramming during pathogen attack ( Pandey and Somssich, 2009 ; Phukan et al., 2016 ), and among them, WRKYs are the most involved TF family in plant defense regulation ( Zhang et al., 2016 ; Yuan et al., 2018 ; Zambounis et al., 2020 ; Xiao et al., 2022 ).…”

“…Previously, it was recorded that 19, 35, and 7 WRKY-encoding genes were involved in the regulation of defense responses in rose petals, grapevine, and strawberry flowers to Botrytis cinerea , respectively ( Haile et al., 2017 ; Liu et al., 2018 ; Xiao et al., 2022 ). TFs are key regulators of the host transcriptional reprogramming during pathogen attack ( Pandey and Somssich, 2009 ; Phukan et al., 2016 ), and among them, WRKYs are the most involved TF family in plant defense regulation ( Zhang et al., 2016 ; Yuan et al., 2018 ; Zambounis et al., 2020 ; Xiao et al., 2022 ). Furthermore, the positive impact of WRKY TFs in rice and Arabidopsis responses to pathogen attacks was further highlighted as WRKYs can functionally cooperate in co-regulatory networks such as in the “COR-A” network ( Berri et al., 2009 ).…”

Strawberry Grey Mould, a Devastating Disease Caused by the Airborne Fungal Pathogen Botrytis cinerea

“…Soil sterilization at 55°C for 15 min proved lethal to Botrytis spp. It is clear that greenhouse conditions are easier to handle with field-grown strawberries, however some other techniques can be applied to both field and greenhouse crops; good soil drainage, putting straw mulches or polythene cover to reduce the plant and soil-surface contact (Legard et al, 2000 andFedele et al, 2020), choosing the correct time and rate of fertilizer applications, weeds management (weeds increase the infection of Botrytis spp., impede air circulation, and can be a source of inoculum), eliminating of rotten strawberries frequently and remove them away (Legard et al, 2000 andWilliamson et al, 2007), planting in raised beds and effective pruning (Legard et al, 2000;Li et al, 2022 andXiao et al, 2022).…”

“…cinerea interaction, the microenvironment and its antagonists on the host plant is essential for a good choice of a control strategy against B. cinerea (Boff et al, 2001;Blanco et al, 2006 andFedele et al, 2020). Although chemical control (Ortuno et al, 2014 andFeliziani andRomanazzi, 2016) and resistant cultivars (Evenhuis andWanten, 2006 andPelayo-Zaldívar et al, 2007) is the mainstays of B. cinerea management, there are other types of management strategies, such as biological control (De Angelis et al, 2022) and cultural activities (Fedele et al, 2020;Li et al, 2022 andXiao et al, 2022).…”