NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula

Katharina Schiessl, Jodi L.S. Lilley, Tak Lee, Ioannis Tamvakis, Wouter Kohlen, Paul C. Bailey, Aaron Thomas, Jakub Luptak, Karunakaran Ramakrishnan, Matthew D. Carpenter, Kirankumar S. Mysore, Jiangqi Wen, Sebastian Ahnert, Veronica A. Grieneisen, Giles E.D. Oldroyd*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

Abstract

To overcome nitrogen deficiencies in the soil, legumes enter symbioses with rhizobial bacteria that convert atmospheric nitrogen into ammonium. Rhizobia are accommodated as endosymbionts within lateral root organs called nodules that initiate from the inner layers of Medicago truncatula roots in response to rhizobial perception. In contrast, lateral roots emerge from predefined founder cells as an adaptive response to environmental stimuli, including water and nutrient availability. CYTOKININ RESPONSE 1 (CRE1)-mediated signaling in the pericycle and in the cortex is necessary and sufficient for nodulation, whereas cytokinin is antagonistic to lateral root development, with cre1 showing increased lateral root emergence and decreased nodulation. To better understand the relatedness between nodule and lateral root development, we undertook a comparative analysis of these two root developmental programs. Here, we demonstrate that despite differential induction, lateral roots and nodules share overlapping developmental programs, with mutants in LOB-DOMAIN PROTEIN 16 (LBD16) showing equivalent defects in nodule and lateral root initiation. The cytokinin-inducible transcription factor NODULE INCEPTION (NIN) allows induction of this program during nodulation through activation of LBD16 that promotes auxin biosynthesis via transcriptional induction of STYLISH (STY) and YUCCAs (YUC). We conclude that cytokinin facilitates local auxin accumulation through NIN promotion of LBD16, which activates a nodule developmental program overlapping with that induced during lateral root initiation.

Original languageEnglish
Pages (from-to)3657-3668.e5
JournalCurrent Biology
Volume29
Issue number21
DOIs
Publication statusPublished - 4 Nov 2019

Fingerprint

Medicago truncatula
Cytokinins
Organogenesis
organogenesis
cytokinins
nodulation
Indoleacetic Acids
auxins
Nitrogen
Rhizobium
ammonium nitrogen
Symbiosis
Biosynthesis
endosymbionts
Ammonium Compounds
Fabaceae
nutrient availability
symbiosis
Nutrients
Bacteria

Keywords

  • auxin
  • CYTOKININ RESPONSE FACTOR
  • endosymbiosis
  • LATERAL ORGAN BOUNDARIES DOMAIN
  • lateral root/nodule organogenesis
  • Medicago truncatula
  • nitrogen
  • NODULE INCEPTION
  • rhizobia
  • YUCCA

Cite this

Schiessl, Katharina ; Lilley, Jodi L.S. ; Lee, Tak ; Tamvakis, Ioannis ; Kohlen, Wouter ; Bailey, Paul C. ; Thomas, Aaron ; Luptak, Jakub ; Ramakrishnan, Karunakaran ; Carpenter, Matthew D. ; Mysore, Kirankumar S. ; Wen, Jiangqi ; Ahnert, Sebastian ; Grieneisen, Veronica A. ; Oldroyd, Giles E.D. / NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula. In: Current Biology. 2019 ; Vol. 29, No. 21. pp. 3657-3668.e5.
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title = "NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula",
abstract = "To overcome nitrogen deficiencies in the soil, legumes enter symbioses with rhizobial bacteria that convert atmospheric nitrogen into ammonium. Rhizobia are accommodated as endosymbionts within lateral root organs called nodules that initiate from the inner layers of Medicago truncatula roots in response to rhizobial perception. In contrast, lateral roots emerge from predefined founder cells as an adaptive response to environmental stimuli, including water and nutrient availability. CYTOKININ RESPONSE 1 (CRE1)-mediated signaling in the pericycle and in the cortex is necessary and sufficient for nodulation, whereas cytokinin is antagonistic to lateral root development, with cre1 showing increased lateral root emergence and decreased nodulation. To better understand the relatedness between nodule and lateral root development, we undertook a comparative analysis of these two root developmental programs. Here, we demonstrate that despite differential induction, lateral roots and nodules share overlapping developmental programs, with mutants in LOB-DOMAIN PROTEIN 16 (LBD16) showing equivalent defects in nodule and lateral root initiation. The cytokinin-inducible transcription factor NODULE INCEPTION (NIN) allows induction of this program during nodulation through activation of LBD16 that promotes auxin biosynthesis via transcriptional induction of STYLISH (STY) and YUCCAs (YUC). We conclude that cytokinin facilitates local auxin accumulation through NIN promotion of LBD16, which activates a nodule developmental program overlapping with that induced during lateral root initiation.",
keywords = "auxin, CYTOKININ RESPONSE FACTOR, endosymbiosis, LATERAL ORGAN BOUNDARIES DOMAIN, lateral root/nodule organogenesis, Medicago truncatula, nitrogen, NODULE INCEPTION, rhizobia, YUCCA",
author = "Katharina Schiessl and Lilley, {Jodi L.S.} and Tak Lee and Ioannis Tamvakis and Wouter Kohlen and Bailey, {Paul C.} and Aaron Thomas and Jakub Luptak and Karunakaran Ramakrishnan and Carpenter, {Matthew D.} and Mysore, {Kirankumar S.} and Jiangqi Wen and Sebastian Ahnert and Grieneisen, {Veronica A.} and Oldroyd, {Giles E.D.}",
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doi = "10.1016/j.cub.2019.09.005",
language = "English",
volume = "29",
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Schiessl, K, Lilley, JLS, Lee, T, Tamvakis, I, Kohlen, W, Bailey, PC, Thomas, A, Luptak, J, Ramakrishnan, K, Carpenter, MD, Mysore, KS, Wen, J, Ahnert, S, Grieneisen, VA & Oldroyd, GED 2019, 'NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula', Current Biology, vol. 29, no. 21, pp. 3657-3668.e5. https://doi.org/10.1016/j.cub.2019.09.005

NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula. / Schiessl, Katharina; Lilley, Jodi L.S.; Lee, Tak; Tamvakis, Ioannis; Kohlen, Wouter; Bailey, Paul C.; Thomas, Aaron; Luptak, Jakub; Ramakrishnan, Karunakaran; Carpenter, Matthew D.; Mysore, Kirankumar S.; Wen, Jiangqi; Ahnert, Sebastian; Grieneisen, Veronica A.; Oldroyd, Giles E.D.

In: Current Biology, Vol. 29, No. 21, 04.11.2019, p. 3657-3668.e5.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula

AU - Schiessl, Katharina

AU - Lilley, Jodi L.S.

AU - Lee, Tak

AU - Tamvakis, Ioannis

AU - Kohlen, Wouter

AU - Bailey, Paul C.

AU - Thomas, Aaron

AU - Luptak, Jakub

AU - Ramakrishnan, Karunakaran

AU - Carpenter, Matthew D.

AU - Mysore, Kirankumar S.

AU - Wen, Jiangqi

AU - Ahnert, Sebastian

AU - Grieneisen, Veronica A.

AU - Oldroyd, Giles E.D.

PY - 2019/11/4

Y1 - 2019/11/4

N2 - To overcome nitrogen deficiencies in the soil, legumes enter symbioses with rhizobial bacteria that convert atmospheric nitrogen into ammonium. Rhizobia are accommodated as endosymbionts within lateral root organs called nodules that initiate from the inner layers of Medicago truncatula roots in response to rhizobial perception. In contrast, lateral roots emerge from predefined founder cells as an adaptive response to environmental stimuli, including water and nutrient availability. CYTOKININ RESPONSE 1 (CRE1)-mediated signaling in the pericycle and in the cortex is necessary and sufficient for nodulation, whereas cytokinin is antagonistic to lateral root development, with cre1 showing increased lateral root emergence and decreased nodulation. To better understand the relatedness between nodule and lateral root development, we undertook a comparative analysis of these two root developmental programs. Here, we demonstrate that despite differential induction, lateral roots and nodules share overlapping developmental programs, with mutants in LOB-DOMAIN PROTEIN 16 (LBD16) showing equivalent defects in nodule and lateral root initiation. The cytokinin-inducible transcription factor NODULE INCEPTION (NIN) allows induction of this program during nodulation through activation of LBD16 that promotes auxin biosynthesis via transcriptional induction of STYLISH (STY) and YUCCAs (YUC). We conclude that cytokinin facilitates local auxin accumulation through NIN promotion of LBD16, which activates a nodule developmental program overlapping with that induced during lateral root initiation.

AB - To overcome nitrogen deficiencies in the soil, legumes enter symbioses with rhizobial bacteria that convert atmospheric nitrogen into ammonium. Rhizobia are accommodated as endosymbionts within lateral root organs called nodules that initiate from the inner layers of Medicago truncatula roots in response to rhizobial perception. In contrast, lateral roots emerge from predefined founder cells as an adaptive response to environmental stimuli, including water and nutrient availability. CYTOKININ RESPONSE 1 (CRE1)-mediated signaling in the pericycle and in the cortex is necessary and sufficient for nodulation, whereas cytokinin is antagonistic to lateral root development, with cre1 showing increased lateral root emergence and decreased nodulation. To better understand the relatedness between nodule and lateral root development, we undertook a comparative analysis of these two root developmental programs. Here, we demonstrate that despite differential induction, lateral roots and nodules share overlapping developmental programs, with mutants in LOB-DOMAIN PROTEIN 16 (LBD16) showing equivalent defects in nodule and lateral root initiation. The cytokinin-inducible transcription factor NODULE INCEPTION (NIN) allows induction of this program during nodulation through activation of LBD16 that promotes auxin biosynthesis via transcriptional induction of STYLISH (STY) and YUCCAs (YUC). We conclude that cytokinin facilitates local auxin accumulation through NIN promotion of LBD16, which activates a nodule developmental program overlapping with that induced during lateral root initiation.

KW - auxin

KW - CYTOKININ RESPONSE FACTOR

KW - endosymbiosis

KW - LATERAL ORGAN BOUNDARIES DOMAIN

KW - lateral root/nodule organogenesis

KW - Medicago truncatula

KW - nitrogen

KW - NODULE INCEPTION

KW - rhizobia

KW - YUCCA

U2 - 10.1016/j.cub.2019.09.005

DO - 10.1016/j.cub.2019.09.005

M3 - Article

VL - 29

SP - 3657-3668.e5

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 21

ER -