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© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
The stigma of death
The stigma has a tightly regulated functional lifespan and is therefore a key determinant for ﬂoral receptivity.
New evidence reveals how two transcription factors play a pivotal role in controlling stigma lifespan by regulating
developmental programmed cell death in this tissue to terminate pollen receptivity.
Maurice Bosch and Noni V. E. Franklin-Tong
uring pollination, complex pollen–
pistil interactions play a decisive role
in determining reproductive success.
The female stigmatic papilla cells are crucial,
acting as the receptive tissue for pollen
grains. Although pollen–pistil interactions
have been studied quite intensively in recent
, we know very little about what
regulates the development of pistil papilla
cells. Stigma receptivity is a key prerequisite
for successful pollination and seed set in
flowering plants. From a plant breeder’s
perspective, extending the length of time
that the stigma can support the germination
and growth of pollen can safeguard seed
production and yield. This is even more
pertinent in the context of food security and
the susceptibility of plant reproduction to
the effects of climate change
Death is one of the greatest mysteries
of life, not least for plants
. Although we
are beginning to understand some of the
processes involved in developmentally
controlled programmed cell death (dPCD)
, many of the components and
processes involved in this crucial decision-
making event remain to be elucidated. In
this issue of Nature Plants, Gao et al.
that a dPCD programme ends the functional
lifespan of unpollinated stigmatic papilla
cells, terminating their receptivity for pollen.
This ground-breaking study shows that a
specific developmental programme controls
stigma lifespan, and identifies two key NAC
transcription factors (NAC TFs), KIRA1
and ORESARA1 (also known as ANAC074
and ANAC092, respectively), that regulate
this process. Although senescence in
unpollinated Arabidopsis thaliana pistils has
been described to some extent
, the study
by Gao et al.
provides the first evidence for
a definitive role for dPCD in controlling
stigma lifespan. This work provides a
substantial contribution to advancing our
understanding in the fields of both plant
reproduction and dPCD research.
The authors characterized dPCD spatially
and temporally using reporter genes, and
provide solid evidence for dPCD in the
stigmatic papillae of maturing A. thaliana
Stage 1 Stage 2 Stage 3 Stage 4
Stigmatic papilla cells
Fig. 1 | dPCD in unpollinated stigmata. a, Time line of dPCD progression. Stigmatic papilla cells
elongate and are fully mature at stage 2. Senescence is initiated at stage 3 and stigma death complete
at stage 4. Consequently, if pollinated at stage 3 or later, significantly reduced seed set is achieved.
b, Within the stigmatic papillae at stage 3, the cells undergo dPCD (inset). Expression of the NAC
transcription factors KIR1 and ORE1 is strongly upregulated and is sufficient to initiate dPCD. KIR1 and
ORE1 can directly activate expression of the dPCD-associated genes RNS3 (ribonuclease 3), BFN1
(bifunctional nuclease 1) and EXI1 (exitus 1). The execution of cell death in individual papilla cells
is completed in about 1 hour. Temporally, the first notable cell-death event is vacuolar collapse,
followed by the loss of plasma membrane integrity, abrupt nuclear disintegration and complete
cellular collapse. Papilla cell death is significantly delayed in loss-of-function mutants for KIR1 and ORE1.
PM, plasma membrane.
NATURE PLANTS | VOL 4 | JUNE 2018 | 323–324 | www.nature.com/natureplants