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A molecular network mediating adventitious root initiation in Arabidopsis thaliana
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). (Catherine Bellini)
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

To adapt to the ever-changing rhizosphere conditions, land plants evolved a sophisticated root system. The genetic determinants of the root system establishment have been the targets of natural selection, resulting in a very complex but robust molecular networks and circuits. These networks provide the plant with precise cell-fate and developmental decisions. The plant root system consists of primary root, lateral roots and often adventitious roots (ARs). ARs derive from the aboveground organs in response to either intrinsic developmental cues or in response to the environmental ones. AR formation is a pre-requisite step for vegetative propagation, which is widely used to multiply elite genotypes in forestry and agriculture. The main focus of this study is to unravel the molecular networks controlling AR initiation (ARI) using the intact-etiolated Arabidopsis hypocotyl as a model system. Previous data from our laboratory showed that ARI in Arabidopsis is controlled by a crosstalk between the positive regulator auxin (IAA) and the negative regulator jasmonate (JA). First, combining genetic, biochemical and hormonomics approaches, we identified the auxin coreceptor complexes involved in ARI. We found that IAA is perceived by two F-box proteins (TRANSPORT INHIBITOR1/AUXIN-SIGNALLING F-BOX (TIR1) and its closest homolog AFB2 as well as three Auxin/Inodole-3-acetic acid (Aux/IAA) repressors (IAA6, IAA9 and IAA17). These coreceptor proteins possibly act in combinatorial manner to fine-tune the auxin signaling machinery during ARI. In addition, in a genetic screen, we also revealed that the COP9 SIGNALOSOME SUBUNIT 4 (CSN4) protein plays a central role in ARI by modulating the function of the auxin perception machinery. Next, in silico search for genes acting downstream of JA involved in ARI, we retrieved the recently characterized DIOXYGENASE FOR AUXIN OXIDATION (DAO1) and DAO2 genes. The DAOs encode for enzymes that catalyze the conversion of free IAA into 2-oxindole-3-acetic acid (oxIAA), a rate-limiting step in auxin degradation. We found that the DAO1 gene mediates a molecular circuit to stabilize the interaction between IAA and JA. Combining genetics, genome-wide transcriptome profiling, hormononics and cell biological approaches, we found that MYC2-mediated JA signaling controls the expression of the ETHYLENE RESPONSE FACTOR 115 (ERF115) gene, which is a repressor of ARI. Our genetic data revealed that ERF115-mediated ARI inhibition requires cytokinins (CKs). CKs have long been established as inhibitors of ARI. Altogether, ARI seems to be controlled by a complex molecular network guided by three hormonal pathways (IAA, JA and CK), in which JA-induced ERF115 plays a role of "molecular switch".

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2019. , p. 52
Keywords [en]
Adventitious rooting, auxin, jasmonate, cytokinin, phytohormone perception and signalling, vegetative propagation
National Category
Developmental Biology
Identifiers
URN: urn:nbn:se:umu:diva-164953ISBN: 9789178551385 (print)OAI: oai:DiVA.org:umu-164953DiVA, id: diva2:1368017
Public defence
2019-11-28, KB.E3.01 (Lilla hörsalen), KBC-huset, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2019-11-07 Created: 2019-11-05 Last updated: 2021-05-24Bibliographically approved
List of papers
1. A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis
Open this publication in new window or tab >>A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis
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2019 (English)In: Molecular Plant, ISSN 1674-2052, E-ISSN 1752-9867, Vol. 12, no 11, p. 1499-1514Article in journal (Refereed) Published
Abstract [en]

In Arabidopsis thaliana, canonical auxin-dependent gene regulation is mediated by 23 transcription factors from the AUXIN RESPONSE FACTOR (ARF) family that interact with auxin/indole acetic acid repressors (Aux/IAAs), which themselves form co-receptor complexes with one of six TRANSPORT INHIBITOR1/AUXIN-SIGNALLING F-BOX (TIR1/AFB) proteins. Different combinations of co-receptors drive specific sensing outputs, allowing auxin to control a myriad of processes. ARF6 and ARF8 are positive regulators of adventitious root initiation upstream of jasmonate, but the exact auxin co-receptor complexes controlling the transcriptional activity of these proteins has remained unknown. Here, using loss-of-function mutants we show that three Aux/IAA genes, IAA6, IAA9, and IAA17, act additively in the control of adventitious root (AR) initiation. These three IAA proteins interact with ARF6 and/or ARF8 and likely repress their activity in AR development. We show that TIR1 and AFB2 are positive regulators of AR formation and TIR1 plays a dual role in the control of jasmonic acid (JA) biosynthesis and conjugation, as several JA biosynthesis genes are up-regulated in the tir1-1 mutant. These results lead us to propose that in the presence of auxin, TIR1 and AFB2 form specific sensing complexes with IAA6, IAA9, and/or IAA17 to modulate JA homeostasis and control AR initiation.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Arabidopsis, AuxIAA, TIR1/AFB, adventitious roots, jasmonate
National Category
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-164949 (URN)10.1016/j.molp.2019.09.001 (DOI)000494946400011 ()31520787 (PubMedID)2-s2.0-85073030581 (Scopus ID)
Funder
Swedish Research CouncilVinnovaKnut and Alice Wallenberg FoundationCarl Tryggers foundation The Kempe Foundations
Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2023-03-23Bibliographically approved
2. The Arabidopsis Cop9 signalosome subunit 4 (CNS4) is involved in adventitious root formation
Open this publication in new window or tab >>The Arabidopsis Cop9 signalosome subunit 4 (CNS4) is involved in adventitious root formation
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2017 (English)In: Scientific Reports, E-ISSN 2045-2322, Vol. 7, article id 628Article in journal (Refereed) Published
Abstract [en]

The COP9 signalosome (CSN) is an evolutionary conserved multiprotein complex that regulates many aspects of plant development by controlling the activity of CULLIN-RING E3 ubiquitin ligases (CRLs). CRLs ubiquitinate and target for proteasomal degradation a vast number of specific substrate proteins involved in many developmental and physiological processes, including light and hormone signaling and cell division. As a consequence of CSN pleiotropic function, complete loss of CSN activity results in seedling lethality. Therefore, a detailed analysis of CSN physiological functions in adult Arabidopsis plants has been hampered by the early seedling lethality of csn null mutants. Here we report the identification and characterization of a viable allele of the Arabidopsis COP9 signalosome subunit 4 (CSN4). The allele, designated csn4-2035, suppresses the adventitious root (AR) phenotype of the Arabidopsis superroot2-1 mutant, potentially by altering its auxin signaling. Furthermore, we show that although the csn4-2035 mutation affects primary and lateral root (LR) formation in the 2035 suppressor mutant, CSN4 and other subunits of the COP9 complex seem to differentially control AR and LR development.

Place, publisher, year, edition, pages
Nature Publishing Group, 2017
National Category
Plant Biotechnology
Identifiers
urn:nbn:se:umu:diva-134205 (URN)10.1038/s41598-017-00744-1 (DOI)000398162600004 ()28377589 (PubMedID)2-s2.0-85017188913 (Scopus ID)
Note

Errata: Pacurar, D.I., Pacurar, M.L., Lakehal, A. et al. Erratum: The Arabidopsis Cop9 signalosome subunit 4 (CSN4) is involved in adventitious root formation. Sci Rep 2017;7:6435. DOI: 10.1038/s41598-017-04861-9

Available from: 2017-06-21 Created: 2017-06-21 Last updated: 2023-07-07Bibliographically approved
3. A DAO1-Mediated Circuit Controls Auxin and Jasmonate Crosstalk Robustness during Adventitious Root Initiation in Arabidopsis
Open this publication in new window or tab >>A DAO1-Mediated Circuit Controls Auxin and Jasmonate Crosstalk Robustness during Adventitious Root Initiation in Arabidopsis
2019 (English)In: International Journal of Molecular Sciences, ISSN 1661-6596, E-ISSN 1422-0067, Vol. 20, no 18, article id 4428Article in journal (Refereed) Published
Abstract [en]

Adventitious rooting is a post-embryonic developmental program governed by a multitude of endogenous and environmental cues. Auxin, along with other phytohormones, integrates and translates these cues into precise molecular signatures to provide a coherent developmental output. Auxin signaling guides every step of adventitious root (AR) development from the early event of cell reprogramming and identity transitions until emergence. We have previously shown that auxin signaling controls the early events of AR initiation (ARI) by modulating the homeostasis of the negative regulator jasmonate (JA). Although considerable knowledge has been acquired about the role of auxin and JA in ARI, the genetic components acting downstream of JA signaling and the mechanistic basis controlling the interaction between these two hormones are not well understood. Here we provide evidence that COI1-dependent JA signaling controls the expression of DAO1 and its closely related paralog DAO2. In addition, we show that the dao1-1 loss of function mutant produces more ARs than the wild type, probably due to its deficiency in accumulating JA and its bioactive metabolite JA-Ile. Together, our data indicate that DAO1 controls a sensitive feedback circuit that stabilizes the auxin and JA crosstalk during ARI.

Place, publisher, year, edition, pages
MDPI, 2019
Keywords
adventitious roots, auxin, auxin oxidation, jasmonates, organogenesis
National Category
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-164948 (URN)10.3390/ijms20184428 (DOI)000489100500107 ()31505771 (PubMedID)2-s2.0-85072026303 (Scopus ID)
Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2023-03-24Bibliographically approved
4. A Jasmonate-mediated molecular network provides cell-reprogramming decisions for organogenesis in Arabidopsis
Open this publication in new window or tab >>A Jasmonate-mediated molecular network provides cell-reprogramming decisions for organogenesis in Arabidopsis
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2019 (English)Manuscript (preprint) (Other academic)
National Category
Developmental Biology
Identifiers
urn:nbn:se:umu:diva-164951 (URN)
Available from: 2019-11-05 Created: 2019-11-05 Last updated: 2019-11-06

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Lakehal, Abdellah

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