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Root regulation of artemisinin production in Artemisia annua: trichome and metabolite evidence

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Abstract

Main conclusion

Roots of plants with high artemisinin-producing leaves increased leaf production of artemisinin in low-producing plants and vice versa indicating roots are involved in controlling artemisinin biosynthesis in shoots.

The anti-malarial sesquiterpene, artemisinin, is produced and stored in glandular trichomes (GLTs) of Artemisia annua. Evidence suggested roots, which produce no significant artemisinin nor precursor compounds, regulate production of artemisinin biosynthesis in the leaves. Using grafting, we studied the relationship between rootstock and scion by measuring GLTs and five artemisinic metabolites (artemisinin, deoxyartemisinin, dihydroartemisinic acid, artemisinic acid, arteannuin B) in scions of ungrafted, self-grafted, and cross-grafted plants among three cultivars: S and 15 both having GLTs with artemisinin at 1.49 and 0.57 %, respectively, and G producing neither GLTs nor detectable artemisinin. All artemisinin-producing self-grafts, e.g., S/S (scion/rootstock) and 15/15, produced more artemisinin than ungrafted plants, likely from grafting stress. S/S grafts also produced more GLTs. The 15/S grafts produced more artemisinin than S/15, suggesting rootstocks from high producing S plants stimulated artemisinin production in 15 scions. S/15 grafts yielded less artemisinin than S/S, but more than either 15/15 or ungrafted n15 and nS; S/15 grafts also had a lower density of GLTs than S/S, suggesting rootstock inhibition of the scion. The S rootstock induced trace artemisinin production in G scions, but did not induce GLT formation in G/S grafts. Different grafts exhibited different trichome morphologies and effects on artemisinic pathway flux. This study provides new information regarding the role of roots in GLT development and artemisinin production in this important medicinal plant.

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Abbreviations

AA:

Artemisinic acid

AAA:

Artemisinic aldehyde

AACT:

Acetoacetyl-CoA thiolase

AAOH:

Artemisinic alcohol

AB:

Arteannuin B

ADS:

Amorpha-4, 11-diene synthase

ALDH1:

Aldehyde dehydrogenase 1

AN:

Artemisinin

CYP:

CYP71AV1, cytochrome P450-dependent hydroxylase

DBR2:

Double bond reductase 2

DHAA:

Dihydroartemisinic acid

DHAAA:

Dihydroartemisinic aldehyde

DHOH:

Dihydroartemisinic alcohol

dAN:

Deoxyartemisinin

FLV:

Flavonoid

FPP:

Farnesyl pyrophosphate

G:

Glandless artemisinin null mutant of A. annua

GLT:

Glandular trichome

RED1:

Dihydroartemisinic aldehyde reductase 1

ROS:

Reactive oxygen species

ShAM:

Shoot apical meristem

S:

SAM cultivar of A. annua

15:

#15 cultivar of A. annua

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Acknowledgments

The authors are grateful for the partial financial support of WPI and the assistance of Dr. Abdul Mannan (COMSATS, Pakistan), and Andy Butler, Hailey Cambra, Dr. Liwen Fei, and Professors Kristen Wobbe and Luis Vidali of WPI for suggestions and technical help on this project.

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  1. Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, MA, USA

    Sibo Wang, Melissa J. Towler & Pamela J. Weathers

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  1. Sibo Wang
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  2. Melissa J. Towler
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  3. Pamela J. Weathers
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Correspondence to Pamela J. Weathers.

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Wang, S., Towler, M.J. & Weathers, P.J. Root regulation of artemisinin production in Artemisia annua: trichome and metabolite evidence. Planta 244, 999–1010 (2016). https://doi.org/10.1007/s00425-016-2560-0

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