© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
VIB Center of Plant Systems Biology, Ghent, Belgium.
Lab of Plant Growth Analysis, Ghent University Global Campus, Yeonsu-gu, Incheon, Republic of Korea.
Laboratory of Food Technology and Engineering,
Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
VIB Center for Inflammation Research, Ghent, Belgium.
Department of Internal
Medicine, Ghent University, Ghent, Belgium.
Department of Pulmonary Medicine, Ersamus MC, Rotterdam, the Netherlands.
Present address: Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China.
Present address: Institute of Science
and Technology (IST), Klosterneuburg, Austria.
These authors contributed equally: Zhen Gao, Anna Daneva. *e-mail: email@example.com;
lowers are short-lived plant organs that facilitate sexual
reproduction in angiosperms. The floral life span is restricted by
pollination-induced floral organ senescence, which is triggered
by seed set and fruit development in many species
. After successful
pollination, hormonal pathways signal that floral organs have
become obsolete and can be disposed of
. However, floral organs
can also start senescing in the absence of pollination after a species-
specific time span that can range from mere hours to several weeks.
The time between flower maturation and onset of unpollinated
flower senescence is known as the effective pollination period
, conveying the concept that the reproductive potential of a
flower is irrevocably lost once flower senescence sets in.
The enormous plasticity of the EPP among plant species sug
gests an active control of this trait. Since the late 1990s, flower
senescence research, using mainly petals as a model system, has
gained insights into the physiology and molecular regulation of
. Abscisic acid and cytokinin influence the petal life
span via a complex crosstalk with ethylene
. Downstream of phy-
tohormone signalling, transcriptional networks control the repro-
gramming of senescent floral tissues
. Among several transcription
factor (TF) families, NAC (Non-Apical Meristem; Arabidopsis
Transcription Activation Factor 1 and 2 (ATAF1 and ATAF2); Cup-
shaped Cotyledon 2) family members represent the largest group of
TFs commonly upregulated in different floral organs in Arabidopsis
. In Japanese morning glory (Ipomoea nil),
suppression of EPHEMERAL1 results in delayed petal senescence
Interestingly, the closely related ORESARA1 (ORE1, also known as
ANAC092) encodes a NAC TF that is commonly upregulated in
senescing Arabidopsis leaves, petals and siliques
. In Arabidopsis,
ORE1 promotes leaf senescence as part of a regulatory network
downstream of ethylene signalling
. Genome-wide transcriptome
profiling studies in different species have revealed that flower senes
cence is associated with the differential expression of numerous
. These genes are probably functional in a range of processes
from nutrient mobilization to the regulation of senescence-induced
programmed cell death (PCD). PCD can be defined as the actively
controlled cessation of a cells vital functions
, marking the end
point of the senescence process
. In plants, diverse forms of PCD
can occur both as a response to biotic and abiotic environmental
stresses (ePCD) and in the course of regular development (dPCD)
While ePCD processes are important for a plants adaptation to
environmental stress, the tight regulation of dPCD is indispensable
for plant growth and successful sexual reproduction
the transcriptional regulation of ePCD and dPCD seems to be
largely independent. Central dPCD-associated genes, including
BIFUNCTIONAL NUCLEASE1 (BFN1), PUTATIVE ASPARTIC
PROTEASE A3 (PASPA3), RIBONUCLEASE3 (RNS3), CYSTEIN
ENDOPEPDITASE 1 (CEP1), DUF 679 MEMBRANE PROTEIN4
(DMP4), and EXITUS1 (EXI1), are commonly upregulated in
diverse dPCD processes, but not differentially regulated during
hypersensitive response PCD
In this study, we investigated the molecular mechanism regu
lating the EPP in unpollinated flowers of Arabidopsis. We focused
on the floral stigma as the primary interface for pollen reception
and the key determinant of floral receptivity. Arabidopsis has a
dry stigma, consisting of more than 200 individual papilla cells
KIRA1 and ORESARA1 terminate flower receptivity
by promoting cell death in the stigma of Arabidopsis
, Anna Daneva
, Yuliya Salanenka
, Matthias Van Durme
, Marlies Huysmans
, Freya De Winter
, Steffen Vanneste
, Mansour Karimi
, Jan Van de Velde
, Davy Van de Walle
, Koen Dewettinck
, Bart N. Lambrecht
Moritz K. Nowack
Flowers have a species-specific functional life span that determines the time window in which pollination, fertilization and seed
set can occur. The stigma tissue plays a key role in flower receptivity by intercepting pollen and initiating pollen tube growth
toward the ovary. In this article, we show that a developmentally controlled cell death programme terminates the functional life
span of stigma cells in Arabidopsis. We identified the leaf senescence regulator ORESARA1 (also known as ANAC092) and the
previously uncharacterized KIRA1 (also known as ANAC074) as partially redundant transcription factors that modulate stigma
longevity by controlling the expression of programmed cell death–associated genes. KIRA1 expression is sufficient to induce
cell death and terminate floral receptivity, whereas lack of both KIRA1 and ORESARA1 substantially increases stigma life span.
Surprisingly, the extension of stigma longevity is accompanied by only a moderate extension of flower receptivity, suggesting
that additional processes participate in the control of the flower’s receptive life span.
NATURE PLANTS | VOL 4 | JUNE 2018 | 365–375 | www.nature.com/natureplants