Overexpression of leucoanthocyanidin reductase or anthocyanidin reductase elevates tannins content and confers cassava resistance to two-spotted spider mite

Qing Chen; Xiao Liang; Chunling Wu; Ying Liu; Xiaoqiang Liu; Huiping Zhao; Kaimian Li; Songbi Chen; Haiyan Wang; Zhiling Han; Mufeng Wu; Xiaowen Yao; Jun Shui; Yang Qiao; Xue Zhan; Yao Zhang

doi:10.3389/fpls.2022.994866

Overexpression of leucoanthocyanidin reductase or anthocyanidin reductase elevates tannins content and confers cassava resistance to two-spotted spider mite

Front Plant Sci. 2022 Aug 18:13:994866. doi: 10.3389/fpls.2022.994866. eCollection 2022.

Authors

Qing Chen^{1

2}, Xiao Liang^{1

2}, Chunling Wu^{1

2}, Ying Liu^{1

2}, Xiaoqiang Liu^{1

2}, Huiping Zhao^{1

2}, Kaimian Li³, Songbi Chen³, Haiyan Wang⁴, Zhiling Han^{1

2}, Mufeng Wu^{1

2}, Xiaowen Yao^{1

2}, Jun Shui^{1

2}, Yang Qiao^{1

2}, Xue Zhan^{1

2}, Yao Zhang^{1

2}

Affiliations

¹ Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture and Rural Affairs, Haikou, Hainan, China.
² Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya, Hainan, China.
³ Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agriculture Sciences, Haikou, China.
⁴ Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical, Haikou, China.

Abstract

The two-spotted spider mite (TSSM) is a destructive cassava pest. Intensive demonstration of resistance mechanism greatly facilitates the creation of TSSM-resistant cassava germplasm. Gene to metabolite network plays a crucial role in modulating plant resistance, but little is known about the genes and related metabolites which are responsible for cassava resistance to TSSM. Here, a highly resistant (HR) and a highly susceptible (HS) cassava cultivar were used, integrative and comparative transcriptomic and metabolomic analyses between these two cultivars after TSSM infestation revealed that several genes and metabolites were closely related and significantly different in abundance. In particular, the expression of leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR) genes showed a high positive correlation with most of the metabolites in the tannin biosynthesis pathway. Furthermore, transgenic cassava lines overexpressing either of the genes elevated tannin concentrations and conferred cassava resistance to TSSM. Additionally, different forms of tannins possessed distinct bioactivity on TSSM, of which total condensed tannins (LC₅₀ = 375.68 mg/l) showed maximum lethal effects followed by procyanidin B1 (LC₅₀ = 3537.10 mg/l). This study accurately targets LAR, ANR and specific tannin compounds as critical genes and metabolites in shaping cassava resistance to TSSM, which could be considered as biomarkers for evaluation and creation of pest-resistant cassava germplasm.

Keywords: anthocyanidin reductase; cassava (Manihot esculenta Crantz); leucoanthocyanidin reductase; resistance mechanism; tannins (condensed); two-spotted spider mite (Tetranychus urticae Koch).