Temperatures during ﬂower bud development affect pollen
germination, self-incompatibility reaction and early fruit
development of clementine (Citrus clementina Hort. ex Tan.)
, A. Gentile
, A. Hedhly
& S. La Malfa
1 Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, Catania, Italy
2 Department of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zurich, Zurich, Switzerland
Climate change; ﬂoral biology; parthenocarpy;
pollen tube growth rate; seedlessness.
G. Distefano, Dipartimento di Agricoltura,
Alimentazione e Ambiente, University of
Catania, 95123 Catania, Italy.
Received: 11 May 2017;
Accepted: 30 October 2017
One of the key environmental factors affecting plant reproductive systems is tempera-
ture. Characterising such effects is especially relevant for some commercially impor-
tant genera such as Citrus. In this genus, failure of fertilisation results in
parthenocarpic fruit development and seedlessness, which is a much-prized character.
Here, we characterise the effects of temperature on ﬂower and ovary development,
and on pollen–pistil interactions in ‘Comune’ clementine (Citrus clementina Hort. ex
We examine ﬂower bud development, in vitro pollen germination and pollen–pistil
interaction at different temperatures (15, 20, 25 or 30 °C). These temperatures span
the range from ‘cold’ to ‘hot’ weather during the ﬂowering season in many citrus-
Temperature had a strong effect on ﬂower and ovary development, pollen germina-
tion, and pollen tube growth kinetics. In particular, parthenocarpic fruit development
(indicated by juice vesicle growth) was initiated early if ﬂowers were exposed to war-
mer temperatures during anthesis.
Exposure to different temperatures during ﬂower bud development also alters expres-
sion of the self-incompatibility reaction. This affects the point in the pistil at which
pollen tube growth is arrested and conﬁrms the role of sub- and supra-optimal tem-
peratures in determining the numbers of pollen tubes reaching the ovary.
The reproductive phase of plants is particularly sensitive to the
effects of global warming, much more so than the vegetative
phase. Together with changes in the geographic distribution of
food crop production, arising from climate change, the tem-
perature sensitivity of their reproductive phases will also likely
present signiﬁcant challenges (Hedhly et al. 2009). In both
temperate and tropical fruit trees, erratic setting of both seeds
and fruits is particularly evident when trees are exposed to sub-
or supra-optimal temperatures during the ﬂowering phase
(Hedhly 2011). A number of studies characterising pollen per-
formance in cultivated and wild species have revealed that pol-
len tube growth, and the likelihood of it fertilising an ovule,
depend not only on the pollen genotype (Snow & Spira 1991)
but also on the genotype of the pistil (Stephenson & Bertin
1983; Willson & Burley 1983; Herrero & Hormaza 1996; Hor-
maza & Herrero 1996, 1999; Mulcahy et al. 1996). There are
also strong effects of environmental factors during ﬂowering –
especially of temperature (Young & Stanton 1990; Stephenson
et al. 1992; J
ohannsson & Stephenson 1998; Hedhly et al. 2009;
Hedhly 2011; Distefano et al. 2012; Bita & Gerats 2013).
Characterising pollen performance and its sensitivity to tem-
perature is especially relevant for some economically important
fruit crops, such as citrus. Here, failure to fertilise the ovules
results in seedlessness when coupled with parthenocarpic fruit
development. Of course, seedlessness is a prized trait in many
fruit crops. We have previously reported that pollen perfor-
mance in the three ancestral citrus species depends not only on
the genotype of the pollen grain but also on the particular
male–female combination and also on genotype–temperature
interactions during the progamic phase (Distefano et al. 2012).
In mandarin and mandarin-like cultivars and their hybrids
(such as clementine), the study of the progamic phase is espe-
cially interesting because, while they predominantly produce
seedless fruit, they do so without total loss of their capacity to
produce seeds when cross-pollinated. The pistil of citrus
undergoes conspicuous changes during the life of the ﬂower.
Most of these changes are developmentally regulated and either
support or constrain pollen tube growth (Distefano et al.
Pollen–pistil interactions and self-incompatibility (SI) reac-
tions have been well characterised in the last few years in many
species. Although signiﬁcant understanding of the processes
underpinning citrus fruit production has been gained, neither
the SI reaction nor the development of parthenocarpic fruits is
completely characterised. Both SI and parthenocarpy in citrus
are relevant traits as they contribute to seedless fruits, which
are of high market value, compared to their seeded equivalents.
Furthermore, the SI reaction in citrus species appears to be
Plant Biology 20 (2018) 191–198 © 2017 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands
Plant Biology ISSN 1435-8603