A remote cis-regulatory region is required for nin expression in the pericycle to initiate nodule primordium formation in medicago truncatula

Jieyu Liu, Luuk Rutten, Erik Limpens, Tjitse Van Der Molen, Robin Van Velzen, Rujin Chen, Yuhui Chen, Rene Geurts, Wouter Kohlen, Olga Kulikova, Ton Bisseling

Research output: Contribution to journalArticleAcademicpeer-review

3 Citations (Scopus)

Abstract

The legume-rhizobium symbiosis results in nitrogen-fixing root nodules, and their formation involves both intracellular infection initiated in the epidermis and nodule organogenesis initiated in inner root cell layers. NODULE INCEPTION (NIN) is a nodule-specific transcription factor essential for both processes. These NIN-regulated processes occur at different times and locations in the root, demonstrating a complex pattern of spatiotemporal regulation. We show that regulatory sequences sufficient for the epidermal infection process are located within a 5 kb region directly upstream of the NIN start codon in Medicago truncatula. Furthermore, we identify a remote upstream cis-regulatory region required for the expression of NIN in the pericycle, and we show that this region is essential for nodule organogenesis. This region contains putative cytokinin response elements and is conserved in eight more legume species. Both the cytokinin receptor 1, which is essential for nodule primordium formation, and the B-type response regulator RR1 are expressed in the pericycle in the susceptible zone of the uninoculated root. This, together with the identification of the cytokinin-responsive elements in the NIN promoter, strongly suggests that NIN expression is initially triggered by cytokinin signaling in the pericycle to initiate nodule primordium formation.

LanguageEnglish
Pages68-83
JournalPlant Cell
Volume31
Issue number1
Early online date1 Jan 2019
DOIs
Publication statusPublished - Jan 2019

Fingerprint

Medicago truncatula
Cytokinins
Nucleic Acid Regulatory Sequences
cytokinins
Organogenesis
organogenesis
Fabaceae
legumes
regulatory sequences
start codon
Rhizobium
Symbiosis
Initiator Codon
response elements
Response Elements
root nodules
epidermis (plant)
Infection
Epidermis
infection

Cite this

@article{48d8ac8a32dc405fbdd91f9a02505c98,
title = "A remote cis-regulatory region is required for nin expression in the pericycle to initiate nodule primordium formation in medicago truncatula",
abstract = "The legume-rhizobium symbiosis results in nitrogen-fixing root nodules, and their formation involves both intracellular infection initiated in the epidermis and nodule organogenesis initiated in inner root cell layers. NODULE INCEPTION (NIN) is a nodule-specific transcription factor essential for both processes. These NIN-regulated processes occur at different times and locations in the root, demonstrating a complex pattern of spatiotemporal regulation. We show that regulatory sequences sufficient for the epidermal infection process are located within a 5 kb region directly upstream of the NIN start codon in Medicago truncatula. Furthermore, we identify a remote upstream cis-regulatory region required for the expression of NIN in the pericycle, and we show that this region is essential for nodule organogenesis. This region contains putative cytokinin response elements and is conserved in eight more legume species. Both the cytokinin receptor 1, which is essential for nodule primordium formation, and the B-type response regulator RR1 are expressed in the pericycle in the susceptible zone of the uninoculated root. This, together with the identification of the cytokinin-responsive elements in the NIN promoter, strongly suggests that NIN expression is initially triggered by cytokinin signaling in the pericycle to initiate nodule primordium formation.",
author = "Jieyu Liu and Luuk Rutten and Erik Limpens and {Van Der Molen}, Tjitse and {Van Velzen}, Robin and Rujin Chen and Yuhui Chen and Rene Geurts and Wouter Kohlen and Olga Kulikova and Ton Bisseling",
year = "2019",
month = "1",
doi = "10.1105/tpc.18.00478",
language = "English",
volume = "31",
pages = "68--83",
journal = "The Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "1",

}

A remote cis-regulatory region is required for nin expression in the pericycle to initiate nodule primordium formation in medicago truncatula. / Liu, Jieyu; Rutten, Luuk; Limpens, Erik; Van Der Molen, Tjitse; Van Velzen, Robin; Chen, Rujin; Chen, Yuhui; Geurts, Rene; Kohlen, Wouter; Kulikova, Olga; Bisseling, Ton.

In: Plant Cell, Vol. 31, No. 1, 01.2019, p. 68-83.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - A remote cis-regulatory region is required for nin expression in the pericycle to initiate nodule primordium formation in medicago truncatula

AU - Liu, Jieyu

AU - Rutten, Luuk

AU - Limpens, Erik

AU - Van Der Molen, Tjitse

AU - Van Velzen, Robin

AU - Chen, Rujin

AU - Chen, Yuhui

AU - Geurts, Rene

AU - Kohlen, Wouter

AU - Kulikova, Olga

AU - Bisseling, Ton

PY - 2019/1

Y1 - 2019/1

N2 - The legume-rhizobium symbiosis results in nitrogen-fixing root nodules, and their formation involves both intracellular infection initiated in the epidermis and nodule organogenesis initiated in inner root cell layers. NODULE INCEPTION (NIN) is a nodule-specific transcription factor essential for both processes. These NIN-regulated processes occur at different times and locations in the root, demonstrating a complex pattern of spatiotemporal regulation. We show that regulatory sequences sufficient for the epidermal infection process are located within a 5 kb region directly upstream of the NIN start codon in Medicago truncatula. Furthermore, we identify a remote upstream cis-regulatory region required for the expression of NIN in the pericycle, and we show that this region is essential for nodule organogenesis. This region contains putative cytokinin response elements and is conserved in eight more legume species. Both the cytokinin receptor 1, which is essential for nodule primordium formation, and the B-type response regulator RR1 are expressed in the pericycle in the susceptible zone of the uninoculated root. This, together with the identification of the cytokinin-responsive elements in the NIN promoter, strongly suggests that NIN expression is initially triggered by cytokinin signaling in the pericycle to initiate nodule primordium formation.

AB - The legume-rhizobium symbiosis results in nitrogen-fixing root nodules, and their formation involves both intracellular infection initiated in the epidermis and nodule organogenesis initiated in inner root cell layers. NODULE INCEPTION (NIN) is a nodule-specific transcription factor essential for both processes. These NIN-regulated processes occur at different times and locations in the root, demonstrating a complex pattern of spatiotemporal regulation. We show that regulatory sequences sufficient for the epidermal infection process are located within a 5 kb region directly upstream of the NIN start codon in Medicago truncatula. Furthermore, we identify a remote upstream cis-regulatory region required for the expression of NIN in the pericycle, and we show that this region is essential for nodule organogenesis. This region contains putative cytokinin response elements and is conserved in eight more legume species. Both the cytokinin receptor 1, which is essential for nodule primordium formation, and the B-type response regulator RR1 are expressed in the pericycle in the susceptible zone of the uninoculated root. This, together with the identification of the cytokinin-responsive elements in the NIN promoter, strongly suggests that NIN expression is initially triggered by cytokinin signaling in the pericycle to initiate nodule primordium formation.

U2 - 10.1105/tpc.18.00478

DO - 10.1105/tpc.18.00478

M3 - Article

VL - 31

SP - 68

EP - 83

JO - The Plant Cell

T2 - The Plant Cell

JF - The Plant Cell

SN - 1040-4651

IS - 1

ER -