Root uptake of cereal benzoxazinoids grants resistance to root-knot nematode invasion in white clover

TY - JOUR

T1 - Root uptake of cereal benzoxazinoids grants resistance to root-knot nematode invasion in white clover

AU - Hama, Jawameer

AU - Fomsgaard, Inge S.

AU - Topalovic, Olivera

AU - Madsen, Mette Vestergård

PY - 2024/5

Y1 - 2024/5

N2 - Plants synthesize a plethora of chemical defence compounds, which vary between evolutionary lineages. We hypothesize that plants evolved the ability to utilize defence compounds synthesized and released by neighbouring heterospecific plants. In two experiments, we incubated clover (Trifolium repens L.) seedlings with individual benzoxazinoid (BX) compounds (2,4-dihydroxy-1,4-benzoxazin-3-one, 2-hydroxy-1,4-benzoxazin-3-one, benzoxazolinone, and 6-methoxy- benzoxazolin-2-one), a group of bioactive compounds produced by cereals, to allow clover BX uptake. Subsequently, we transplanted the seedlings into soil and quantified BX root and shoot content and invasion of root-knot nematodes in clover roots up to 8 weeks after transplantation. We show that clover root uptake of BXs substantially enhanced clover's resistance against the root-knot nematode Meloidogyne incognita. This effect lasted up to 6 weeks after the clover roots were exposed to the BXs. BXs were absorbed by clover roots, and then translocated to the shoots. As a result of clover metabolization, we detected the parent BXs and a range of their transformation products in the roots and shoots. Based on these novel findings, we envisage that co-cultivation of crop species with complementary and transferable chemical defence systems can add to plant protection.

AB - Plants synthesize a plethora of chemical defence compounds, which vary between evolutionary lineages. We hypothesize that plants evolved the ability to utilize defence compounds synthesized and released by neighbouring heterospecific plants. In two experiments, we incubated clover (Trifolium repens L.) seedlings with individual benzoxazinoid (BX) compounds (2,4-dihydroxy-1,4-benzoxazin-3-one, 2-hydroxy-1,4-benzoxazin-3-one, benzoxazolinone, and 6-methoxy- benzoxazolin-2-one), a group of bioactive compounds produced by cereals, to allow clover BX uptake. Subsequently, we transplanted the seedlings into soil and quantified BX root and shoot content and invasion of root-knot nematodes in clover roots up to 8 weeks after transplantation. We show that clover root uptake of BXs substantially enhanced clover's resistance against the root-knot nematode Meloidogyne incognita. This effect lasted up to 6 weeks after the clover roots were exposed to the BXs. BXs were absorbed by clover roots, and then translocated to the shoots. As a result of clover metabolization, we detected the parent BXs and a range of their transformation products in the roots and shoots. Based on these novel findings, we envisage that co-cultivation of crop species with complementary and transferable chemical defence systems can add to plant protection.

KW - Co-cropping

KW - Defence metabolites

KW - LC-MS/MS

KW - Meloidogyne

KW - Metabolization

KW - Neighbour effects

KW - Trifolium

KW - Edible Grain/parasitology

KW - Disease Resistance

KW - Tylenchoidea/physiology

KW - Plant Diseases/parasitology

KW - Animals

KW - Trifolium/metabolism

KW - Plant Shoots/metabolism

KW - Benzoxazines/metabolism

KW - Plant Roots/parasitology

UR - http://www.scopus.com/inward/record.url?scp=85190727640&partnerID=8YFLogxK

U2 - 10.1016/j.plaphy.2024.108636

DO - 10.1016/j.plaphy.2024.108636

M3 - Journal article

C2 - 38657547

SN - 0981-9428

VL - 210

JO - Plant Physiology and Biochemistry

JF - Plant Physiology and Biochemistry

M1 - 108636

ER -