Induction of defense in cereals by 4-fluorophenoxyacetic acid suppresses insect pest populations and increases crop yields in the field

Wanwan Wang, Pengyong Zhou, Xiaochang Mo, Lingfei Hu,  Nuo Jin, Xia Chen, Zhuoxian Yu, Jinpeng Meng,  Matthias Erb, Zhicai Shang, Angharad M. R. Gatehouse, Jun Wu, and Yonggen Lou

PNAS June 2, 2020 117 (22) 12017-12028

Significance

The exploitation of induced plant defenses for pest control is a promising strategy to reduce the use of pesticides in agriculture. We describe how a newly identified plant strengthener, 4-fluorophenoxyacetic acid (4-FPA), enhances the resistance of rice and other major cereals to sap-sucking insects by triggering the formation of flavonoid polymers in plant cells. We demonstrate that the application of 4-FPA suppresses the population densities of the white-backed planthopper and thereby increases rice yield in the field. This study reveals a mechanism by which plants resist piercing and sucking herbivores and opens avenues for the design of a sustainable generation of plant strengtheners to control insect pests in agriculture.

Abstract

Synthetic chemical elicitors, so called plant strengtheners, can protect plants from pests and pathogens. Most plant strengtheners act by modifying defense signaling pathways, and little is known about other mechanisms by which they may increase plant resistance. Moreover, whether plant strengtheners that enhance insect resistance actually enhance crop yields is often unclear. Here, we uncover how a mechanism by which 4-fluorophenoxyacetic acid (4-FPA) protects cereals from piercing-sucking insects and thereby increases rice yield in the field. Four-FPA does not stimulate hormonal signaling, but modulates the production of peroxidases, H₂O₂, and flavonoids and directly triggers the formation of flavonoid polymers. The increased deposition of phenolic polymers in rice parenchyma cells of 4-FPA-treated plants is associated with a decreased capacity of the white-backed planthopper (WBPH) Sogatella furcifera to reach the plant phloem. We demonstrate that application of 4-PFA in the field enhances rice yield by reducing the abundance of, and damage caused by, insect pests. We demonstrate that 4-FPA also increases the resistance of other major cereals such as wheat and barley to piercing-sucking insect pests. This study unravels a mode of action by which plant strengtheners can suppress herbivores and increase crop yield. We postulate that this represents a conserved defense mechanism of plants against piercing-sucking insect pests, at least in cereals.

See https://www.pnas.org/content/117/22/12017

Figure 1: Four-FPA inhibits root growth and reduces the survival rate of WBPH nymphs. (A and B) Mean survival rate (+SE, n = 8) of 15 newly hatched WBPH nymphs fed on plants that had been grown in nutrient solution with 0 to 5 mg L⁻¹ 4-FPA for 12 h (A); or that had been sprayed with 4 mL of 0 to 100 mg L⁻¹ 4-FPA for 12 h (B); 1 to 8 d after exposure. (C) Growth phenotypes of plants grown in nutrient solution containing 0 to 5 mg L⁻¹ 4-FPA for 10 d. (D and E) Mean root mass (+SE, n = 15) (D); and root length (+SE, n = 15) (E) of plants grown in nutrient solution containing 0 to 5 mg L⁻¹ 4-FPA for 10 d. Asterisks indicate significant differences between treatments and controls (*P < 0.05, **P < 0.01, Duncan’s multiple range test). Upper indicates treatment methods of 4-FPA and its structure.