Integrated analysis of transcriptome, metabolome, and histochemistry reveals the response mechanisms of different ages Panax notoginseng to root-knot nematode infection

Zhuhua Wang; Wenpeng Wang; Wentao Wu; Huiling Wang; Shuai Zhang; Chen Ye; Liwei Guo; Zhaoxia Wei; Hongping Huang; Yixiang Liu; Shusheng Zhu; Youyong Zhu; Yang Wang; Xiahong He

doi:10.3389/fpls.2023.1258316

Integrated analysis of transcriptome, metabolome, and histochemistry reveals the response mechanisms of different ages Panax notoginseng to root-knot nematode infection

Front Plant Sci. 2023 Sep 14:14:1258316. doi: 10.3389/fpls.2023.1258316. eCollection 2023.

Authors

Zhuhua Wang¹, Wenpeng Wang^{1

2}, Wentao Wu¹, Huiling Wang¹, Shuai Zhang¹, Chen Ye¹, Liwei Guo¹, Zhaoxia Wei¹, Hongping Huang¹, Yixiang Liu¹, Shusheng Zhu¹, Youyong Zhu¹, Yang Wang¹, Xiahong He^{1

3}

Affiliations

¹ State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, Yunnan, China.
² Academy of Science and Technology, Chuxiong Normal University, Chuxiong, Yunnan, China.
³ School of Landscape and Horticulture, Southwest Forestry University, Kunming, Yunnan, China.

Abstract

Panax notoginseng (P. notoginseng) is an invaluable perennial medicinal herb. However, the roots of P. notoginseng are frequently subjected to severe damage caused by root-knot nematode (RKN) infestation. Although we have observed that P. notoginseng possessed adult-plant resistance (APR) against RKN disease, the defense response mechanisms against RKN disease in different age groups of P. notoginseng remain unexplored. We aimed to elucidate the response mechanisms of P. notoginseng at different stages of development to RKN infection by employing transcriptome, metabolome, and histochemistry analyses. Our findings indicated that distinct age groups of P. notoginseng may activate the phenylpropanoid and flavonoid biosynthesis pathways in varying ways, leading to the synthesis of phenolics, flavonoids, lignin, and anthocyanin pigments as both the response and defense mechanism against RKN attacks. Specifically, one-year-old P. notoginseng exhibited resistance to RKN through the upregulation of 5-O-p-coumaroylquinic acid and key genes involved in monolignol biosynthesis, such as PAL, CCR, CYP73A, CYP98A, POD, and CAD. Moreover, two-year-old P. notoginseng enhanced the resistance by depleting chlorogenic acid and downregulating most genes associated with monolignol biosynthesis, while concurrently increasing cyanidin and ANR in flavonoid biosynthesis. Three-year-old P. notoginseng reinforced its resistance by significantly increasing five phenolic acids related to monolignol biosynthesis, namely p-coumaric acid, chlorogenic acid, 1-O-sinapoyl-D-glucose, coniferyl alcohol, and ferulic acid. Notably, P. notoginseng can establish a lignin barrier that restricted RKN to the infection site. In summary, P. notoginseng exhibited a potential ability to impede the further propagation of RKN through the accumulation or depletion of the compounds relevant to resistance within the phenylpropanoid and flavonoid pathways, as well as the induction of lignification in tissue cells.

Keywords: Panax notoginseng; lignin; metabolome; phenylpropanoid pathways; root-knot nematode; transcriptome.

Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Key R&D Program of China (2021YFD1000204), the China Agriculture Research System (CARS-21), the Major Science and Technology Project of Yunnan and Kunming (202102AE090042 and 2021JH002), the National Natural Science Foundation of China (32160618), and the Special Basic Cooperative Research Programs of Yunnan Provincial Undergraduate Universities’ Association (202101BA070001-058), the Natural Science Foundation of Yunnan Province (202301BD070001-022), and the Scientific Research Fund Project of Education Department of Yunnan Province (2022J0832).