Journal of Experimental Botany, Vol. 66, No. 23, pp.
9–10, 2015
doi:10.1093/jxb/erv072 
SUPPLEMENT PAPER
My favourite flowering image: floral organs with trichomes
Frank Wellmer*, Darragh Stewart and Diarmuid S. O’Maoileidigh
Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland
* To whom correspondence should be addressed. E-mail: wellmerf@tcd.ie
Received 20 January 2015; Accepted 28 January 2015
Abstract
There is now ample genetic evidence that floral organs are in essence modified leaves, and that floral organ iden-
tity factors are instrumental in the conversion of leaves into floral organs. This idea is exemplified by flowers of
Arabidopsis thaliana that form trichomes on reproductive floral organs as a consequence of a perturbation of the
activity of floral organ identity factors.
In 1790, Johann Wolfgang von Goethe published his semi-
nal essay Metamorphosis of Plants in which he proposed that
the above-ground organs of a plant are derived (‘metamor-
phosed’) from leaves (von Goethe, 1790). Over the years,
much experimental support for this idea has been garnered,
at least for flowers. When the floral organ identity genes were
discovered and studied through genetic analysis, it was found
that the combined loss of several of these genes led to flow-
ers in which floral organs were replaced by leaf-like structures
(Bowman et  al., 1991). Also, it has been reported that the
ectopic expression of specific combinations of floral organ
identity genes leads to the transformation of rosette or caul-
ine leaves into specific floral organ types (Honma and Goto,
2001; Pelaz et  al., 2001). Thus, these genes are clearly nec-
essary and sufficient for the conversion of leaves into floral
organs.
The molecular mechanisms underlying the activity of the
transcription factors, which are encoded by the floral organ
identity genes, have long remained enigmatic. However, in
recent years, the use of transcriptomics experiments and
genome-wide localization studies led to first detailed and
global insights into their functions (Gomez-Mena et al., 2005;
Ito et al., 2004; Kaufmann et al., 2009; Kaufmann et al., 2010;
O Maoileidigh et al., 2013; Pajoro et al., 2014; Wellmer et al.,
2006; Wuest et  al., 2012; Yant et  al., 2010). One of the key
findings of this work was that target genes of the floral organ
identity factors are highly enriched for genes with regulatory
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functions. These include genes that code for microRNAs, tran-
scription factors and for other regulatory proteins. Many of
these regulatory genes had been previously identified through
genetic screens to play important roles during flower forma-
tion. However, there are notable exceptions. When we studied
the activities of the floral organ identity factors APETALA3,
PISTILLATA and AGAMOUS (AG), we found that several
known regulators of leaf development were among the direct
targets (O Maoileidigh et al., 2013; Wuest et al., 2012). These
included genes involved in the formation of trichomes, which
in Arabidopsis are mainly present on leaves and on the inflo-
rescence stem. We then asked whether the floral organ identity
factors are involved in directly repressing trichome formation
on floral organs, which – with the exception of sepals - are tri-
chomeless. Indeed, when we perturbed the activity of AG using
an artificial microRNA approach, we found that trichomes
started to form on the valves of carpels (O Maoileidigh et al.,
2013) . This effect was exacerbated when we conducted the
knockdown of AG in a background in which the repressor of
trichome formation, TRIPTYCHON, is mutated (Figure 1).
These results show that one key feature of leaf development
is directly repressed by a floral organ identity factor. Whether
other aspects of leaf morphogenesis are also directly modi-
fied or suppressed by these transcription factors is currently
unknown, but the number of regulators of leaf development
that act downstream of the floral organ identity factors make
this rather likely in our opinion.
10  | Wellmer et al.
Fig. 1.  A flower of a triptychon mutant, in which AG activity has been perturbed through an artificial microRNA at intermediate stages of development.
Trichomes are forming on carpel valves. Sepals and petals have been removed for better visibility of the reproductive floral organs.
References
Bowman JL, Smyth DR, Meyerowitz EM. 1991. Genetic interactions
among floral homeotic genes of Arabidopsis. Development 112, 1–20.
Gomez-Mena C, de Folter S, Costa MM, Angenent GC, Sablowski
R. 2005. Transcriptional program controlled by the floral homeotic gene
AGAMOUS during early organogenesis. Development 132, 429–438.
Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient
to convert leaves into floral organs. Nature 409, 525–529.
Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann
JL, Meyerowitz EM. 2004. The homeotic protein AGAMOUS controls
microsporogenesis by regulation of SPOROCYTELESS. Nature 430, 356–360.
Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak
C, Krajewski P, Angenent GC. 2009. Target genes of the MADS
transcription factor SEPALLATA3: integration of developmental and
hormonal pathways in the Arabidopsis flower. PLoS Biology 7, e1000090.
Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar
V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM,
Angenent GC, Riechmann JL. 2010. Orchestration of floral initiation by
APETALA1. Science 328, 85–89.
O Maoileidigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT,
Kwasniewska K, Das P, Lohan AJ, Loftus B, Graciet E, Wellmer F.
2013. Control of reproductive floral organ identity specification in Arabidopsis
by the C function regulator AGAMOUS. The Plant Cell 25, 2482–2503.
Pajoro A, Madrigal P, Muino JM, Matus JT, Jin J, Mecchia MA,
Debernardi JM, Palatnik JF, Balazadeh S, Arif M, O’Maoileidigh DS,
Wellmer F, Krajewski P, Riechmann JL, Angenent GC, Kaufmann K.
2014. Dynamics of chromatin accessibility and gene regulation by MADS-
domain transcription factors in flower development. Genome Biology 15,
R41.
Pelaz S, Tapia-Lopez R, Alvarez-Buylla ER, Yanofsky MF. 2001.
Conversion of leaves into petals in Arabidopsis. Current Biology 11,
182–184.
von Goethe JW. 1790. Versuch die Metamorphose der Pflanzen zu
erklären . Gotha, Germany: Ettinger.
Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz
EM. 2006. Genome-wide analysis of gene expression during early
Arabidopsis flower development. PLoS Genetics 2, e117.
Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli
A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F. 2012.
Molecular basis for the specification of floral organs by APETALA3 and
PISTILLATA. Procedings of the National Academy of Sciences U S A 109,
13452–13457.
Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen
X, Schmid M. 2010. Orchestration of the floral transition and floral
development in Arabidopsis by the bifunctional transcription factor
APETALA2. The Plant Cell 22, 2156–2170.