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A novel, semi-dominant allele of MONOPTEROS provides insight into leaf initiation and vein pattern formation

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Abstract

Leaf vein pattern is proposed to be specified by directional auxin transport through presumptive vein cells. Activation of auxin response, which induces downstream genes that entrain auxin transport and lead to vascular differentiation, occurs through a set of transcription factors, the auxin response factors. In the absence of auxin, auxin response factors are inactive because they interact with repressor proteins, the Aux/IAA proteins. One member of the auxin response factor protein family, Auxin Response Factor 5/MONOPTEROS (MP), is critical to vein formation as indicated by reduced vein formation in loss-of-function MP alleles. We have identified a semi-dominant, gain-of-function allele of MP, autobahn or mp abn, which results in vein proliferation in leaves and cotyledons. mp abn is predicted to encode a truncated product that lacks domain IV required for interaction with its Aux/IAA repressor BODENLOS (BDL). We show that the truncated product fails to interact with BDL in yeast two-hybrid assays. Ectopic expression of MP targets including the auxin efflux protein PINFORMED1 (PIN1) further supports the irrepressible nature of mp abn. Asymmetric PIN1:GFP cellular localization does not occur within the enlarged PIN1:GFP expression domains, suggesting the asymmetry requires differential auxin response in neighbouring cells. Organ initiation from mp abn meristems is altered, consistent with disruption to source/sink relationships within the meristem and possible changes in gene expression. Finally, mp abn anthers fail to dehisce and their indehiscence can be relieved by jasmonic acid treatment, suggesting a specific role for MP in late anther development.

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Abbreviations

abn :

autobahn

AP1 :

APETALA1

AP3 :

APETALA3

ARF:

Auxin response factor

ARF5:

AUXIN RESPONSE FACTOR 5

ATHB8 :

ARABIDOPSIS THALIANA HOMEOBOX 8

Aux/IAA:

Auxin/indole-3-acetic acid

BDL :

BODENLOS (also known as IAA12)

BP :

BREVIPEDICELLUS

Col:

Columbia accession

CUC2:

CUP-SHAPED COTYLEDON 2

DAG:

Days after germination

DR5:GUS :

Direct repeat of 5 auxin response elements fused to GUS

FEV:

Freely ending veins

GAL4 :

GALACTOSE4

GAL4-DB:

GAL4-DNA binding domain

GAL4-TA:

GAL4 transcription activation domain

gl1-1 :

glabrous1-1

GFP:

Green fluorescent protein

GUS :

β -glucuronidase

IAA12:

Indole-3-acetic acid 12

IAA13:

Indole-3-acetic acid 13

JA:

Jasmonic acid

KNOX :

KNOTTED-LIKE HOMEOBOX

Ler:

Landsberg erecta accession

LFY :

LEAFY

MP :

MONOPTEROS (also known as ARF5)

NOA:

1-Naphthoxyacetic acid

NPA:

Naphthylphthalamic acid

NPH4:

NON-PHOTOTROPHIC HYPOCOTYL 4

PID :

PINOID

PIN1 :

PINFORMED1

SEM:

Scanning electron microscopy

SHR :

SHORTROOT

STM :

SHOOT MERISTEMLESS

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Acknowledgments

We thank Arabidopsis Biological Resource Center (Columbus, Ohio), Thomas Berleth (University of Toronto, Toronto, ON), George Haughn (Department of Botany, University of British Columbia, Vancouver, BC), Gerd Jürgens (Eberhard-Karls Universität, Tübingen) Giorgio Morelli (Istituto Nazionale della Nutrizione, Rome) and Jane Murfet (University of Missouri, Columbia, MO) for seed donations. This work was funded by a Discovery Grant (E.S.), Post-Graduate Scholarships-Masters (J.J.G.) and Undergraduate Summer Research Awards (M.M., M.B., L.B.) from the Natural Science and Engineering Research Council.

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  1. Department of Biological Sciences, University of Lethbridge, Lethbridge, AB, TIK 3M4, Canada

    Jasmine J. T. Garrett, Miranda J. Meents, Michael T. Blackshaw, LeeAnna C. Blackshaw, Hongwei Hou & Elizabeth A. Schultz

  2. Department of Biology, University of Western Ontario, London, ON, N6A 5B7, Canada

    Danielle M. Styranko & Susanne E. Kohalmi

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  1. Jasmine J. T. Garrett
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Correspondence to Elizabeth A. Schultz.

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M. T. Blackshaw and L. C. Blackshaw contributed equally to the work.

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Garrett, J.J.T., Meents, M.J., Blackshaw, M.T. et al. A novel, semi-dominant allele of MONOPTEROS provides insight into leaf initiation and vein pattern formation. Planta 236, 297–312 (2012). https://doi.org/10.1007/s00425-012-1607-0

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