A comparative analysis of morphology, microstructure, and volatile metabolomics of leaves at varied developmental stages in Ainaxiang (Blumea balsamifera (Linn.) DC.)

Xiaolu Chen; Yanqun Li; Yuxin Pang; Wanyun Shen; Qilei Chen; Liwei Liu; Xueting Luo; Zhenxia Chen; Xingfei Li; Yulan Li; Yingying Zhang; Mei Huang; Chao Yuan; Dan Wang; Lingliang Guan; Yuchen Liu; Quan Yang; Hubiao Chen; Hong Wu; Fulai Yu

doi:10.3389/fpls.2023.1285616

A comparative analysis of morphology, microstructure, and volatile metabolomics of leaves at varied developmental stages in Ainaxiang (Blumea balsamifera (Linn.) DC.)

Front Plant Sci. 2023 Nov 14:14:1285616. doi: 10.3389/fpls.2023.1285616. eCollection 2023.

Authors

Xiaolu Chen^#¹, Yanqun Li^#², Yuxin Pang^#^{1

3}, Wanyun Shen^{1

3}, Qilei Chen⁴, Liwei Liu^{1

5}, Xueting Luo^{1

6}, Zhenxia Chen¹, Xingfei Li¹, Yulan Li¹, Yingying Zhang¹, Mei Huang¹, Chao Yuan¹, Dan Wang¹, Lingliang Guan¹, Yuchen Liu³, Quan Yang⁵, Hubiao Chen⁴, Hong Wu², Fulai Yu¹

Affiliations

¹ Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences/Key Laboratory of Biology and Cultivation of Herb Medicine (Haikou), Ministry of Agriculture and Rural Affairs/Hainan Provincial Engineering Research Center for Blumea balsamifera, Haikou, China.
² Medicinal Plants Research Center, South China Agricultural University, Guangzhou, China.
³ School of Pharmacy, Guizhou University of Traditional Chinese Medicine, Guiyang, China.
⁴ School of Chinese Medicine, Hong Kong Baptist University, Hong Kong, Hong Kong SAR, China.
⁵ School of Traditional Chinese Medicine, Guangdong Pharmaceutical University, Guangzhou, China.
⁶ College of Tropical Crops, Yunnan Agricultural University, Puer, China.

^# Contributed equally.

Abstract

Introduction: Ainaxiang (Blumea balsamifera (Linn.) DC.) is cultivated for the extraction of (-)-borneol and other pharmaceutical raw materials due to its abundant volatile oil. However, there is limited knowledge regarding the structural basis and composition of volatile oil accumulation in fresh B. balsamifera leaves.

Methods: To address this problem, we compare the fresh leaves' morphology, microstructure, and volatile metabonomic at different development stages, orderly defined from the recently unfolded young stage (S1) to the senescent stage (S4).

Results and discussion: Distinct differences were observed in the macro-appearance and microstructure at each stage, particularly in the B. balsamifera glandular trichomes (BbGTs) distribution. This specialized structure may be responsible for the accumulation of volatile matter. 213 metabolites were identified through metabolomic analysis, which exhibited spatiotemporal accumulation patterns among different stages. Notably, (-)-borneol was enriched at S1, while 10 key odor metabolites associated with the characteristic balsamic, borneol, fresh, and camphor aromas of B. balsamifera were enriched in S1 and S2. Ultra-microstructural examination revealed the involvement of chloroplasts, mitochondria, endoplasmic reticulum, and vacuoles in the synthesizing, transporting, and storing essential oils. These findings confirm that BbGTs serve as the secretory structures in B. balsamifera, with the population and morphology of BbGTs potentially serving as biomarkers for (-)-borneol accumulation. Overall, young B. balsamifera leaves with dense BbGTs represent a rich (-)-borneol source, while mesophyll cells contribute to volatile oil accumulation. These findings reveal the essential oil accumulation characteristics in B. balsamifera, providing a foundation for further understanding.

Keywords: Asteraceae; GC-MS; chloroplast; development; fresh leaf; glandular secretory trichomes; terpene; volatile.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the National Natural Science Foundation of China (81603245, 82074123), the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (1630032022022; 1630032022008), the Natural Science Foundation of Hainan Province (2019RC310), and the Innovation and Technology Fund in Hong Kong (MHP/023/20).