Advances in S gene targeted genome-editing and its applicability to disease resistance breeding in selected Solanaceae crop plants

ABSTRACT

Genome-editing tools for the development of traits to tolerate abiotic and biotic adversaries are the recently devised breeding techniques revolutionizing molecular breeding by addressing the issues of rapidness and precision. To that end, disease resistance development by disrupting disease susceptibility genes (S genes) to intervene in the biological mechanism of pathogenicity has significantly improved the techniques of molecular breeding. Despite the achievements in genome-editing aimed at the intervention of the function of susceptibility determinants or gene regulatory elements, off-target effects associated with yield-related traits are still the main setbacks. The challenges are attributed to the complexity of the inheritance of traits controlled by pleiotropic genes. Therefore, a more rigorous genome-editing tool with ultra-precision and efficiency for the development of broad-spectrum and durable disease resistance applied to staple crop plants is of critical importance in molecular breeding programs. The main objective of this article is to review the most impressive progresses achieved in resistance breeding against the main diseases of three Solanaceae crops (potato, Solanum tuberosum; tomato, Solanum lycopersicum and pepper, Capsicum annuum) using genome-editing by disrupting the sequences of S genes, their promoters, or pathogen genes. In this paper, we discussed the complexity and applicability of genome-editing tools, summarized the main disease of Solanaceae crops, and compiled the recent reports on disease resistance developed by S-gene silencing and their off-target effects. Moreover, GO count and gene annotation were made for pooled S-genes from biological databases. Achievements and prospects of S-gene-based next-generation breeding technologies are also discussed.

Highlights

• Most S genes are membrane –anchored and are involved in infection and pre-penetration process

• S gene-editing is less likely to cause an off-target effect

• Gene-editing has been considered a more acceptable engineering tool

• Editing S genes either from the pathogen or host ends has opened new possibilities

KEYWORDS:

• Susceptibility
• solanaceae
• mutagenesis
• effector
• pathogenicity

Future prospects

Genome-editing has presented unprecedented precision and high throughput manipulation of complex genomes which are the main tackles in classical and molecular breeding. Since the first generation of genome-editing with ZFN, CRISPR/Cas variants are now enabling editing of virtually any sequence of interest for different breeding objectives as the genomes of almost all crop plants are sequenced and openly accessible. Despite all the endeavors so far, however, the off-target effects are the main hurdle characterizing S gene editing for the development of disease resistance. The next decade is expected to see a high throughput identification of pleiotropic genes and alternative genome-editing approaches such as targeting S genes with minor off-target effects. The use of tissue or temporal specific promoters in multiplexed CRISPR/Cas gene construct could also minimize the off-target effects associated with yield and other important agronomic traits.

Acknowledgements

The authors acknowledge the College of Agricultural Life Science, Jeonbuk National University, Republic of South Korea. The authors thank Dr. M. Naimuddin for critical reading of the manuscript.

Data availability statement

All the data that support the analysis of the present paper can be available upon reasonable request from the corresponding author.

Ethical approval

As the study did not involve human participants, ethical approval was not required. Ethical approval was exempted by the Department of Applied Biology Department Research Ethics Committee (REC).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21655979.2022.2099599

Additional information

Funding

This study was supported by the National Research Foundation of Korea (NRF), a fund from the Korean Government Ministry of Science and ICT (MSIT) (grant No. NRF-2018R1C1B6002688).