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Safe sex in plants
Flowers are designed to attract animal visitors. Consequently, floral organs are exposed to the microbes carried by their visitors as
well as the microbes transported in air and rain. This is particularly problematic because the nectar, stigmas and the
transmitting tissue of styles are especially rich sources of nutrients, energy and water for the growth of microbes. Not
surprisingly, many pathogens are known to invade plants via the
nectaries and sexual organs of flowers and some pathogens are
specifically adapted to be dispersed from plant to plant by floral
visitors (Antonovics, 2005). So how do plants protect themselves
(and their developing offspring) from the hoard of pathogens that
could invade through floral organs? In an elegant study in this
issue of New Phytologist, Huang et al. (pp. 997–1008) show that
a volatile organic compound (VOC), (E )-b-caryophyllene, that
is produced by the stigmas of Arabidopsis thaliana flowers, acts as
a fumigant that limits the growth of bacterial pathogens such as
Pseudomonas syringae pv. tomato (PST).
mas were not inoculated with PST. In short, (E )-b-caryophyllene
seems to protect the plants from invading bacteria and that the
pathogens, if unchecked at the stigma, adversely affect offspring
quality. To strengthen these findings, they used transgenic plants
that produced extra (E )-b-caryophyllene in the leaves. When the
transgenic and wild-type plants were sprayed with PST, proliferation of the bacteria was greater on the wild-type plants and the
wild-type plants had more necrotic lesions than the transgenic
plants. These findings were consistent with the results of their
stigma infection experiment: (E )-b-caryophyllene increases plant
resistance to a bacterial pathogen. But, does (E )-b-caryophyllene
have anti-microbial properties or does it signal to the plant to
up-regulate other anti-microbial defenses? To answer these questions, Huang et al. cultured PST in liquid media with and
without minute quantities of (E )-b-caryophyllene and they
cultured PST on solid media and added minute quantities of
(E )-b-caryophyllene to the air passing over these cultures. In
both cases, bacterial growth was reduced in a dose dependent
manner by (E )-b-caryophyllene. Finally, they performed a series
of experiments using quantitative real-time PCR to show that
other anti-herbivore and anti-pathogen defense related genes
were not up-regulated by (E )-b-caryophyllene in A. thaliana. In
short, the production of (E )-b-caryophyllene on the stigmas of
A. thaliana plants functions as a direct defense against bacterial
pathogens.
‘But, does ( E)-b-caryophyllene have anti-microbial
properties or does it signal to the plant to up-regulate
other anti-microbial defenses?’
PST is an important bacterial pathogen of tomato and plants
in the cabbage family, such as Arabidopsis thaliana, that causes
necrotic lesions on leaves but such damage is only occasionally
seen on flowers. (E )-b-Caryophyllene is one of the most common compounds found in floral odors, but interestingly, it has
never been shown to function in pollinator attraction (Huang
et al.). Huang et al. used A. thaliana plants that were incapable
of producing (E )-b-caryophyllene due to a transposon insertion
into a key gene in the pathway leading to (E )-b-caryophyllene
synthesis and inoculated the stigmas of these mutant plants and
wild-type plants with PST. They found that the bacteria had
greater proliferation and produced more symptoms on the
mutant plants. Moreover, the seeds resulting from the mutants
weighed less and were misshapen compared with wild-type plants
but there were no differences in seed characteristics when the stig 2012 The Author
New Phytologist 2012 New Phytologist Trust
Floral traits are influenced by many selective
pressures
Pollination biology and floral ecology historically have been concerned with the effects of floral traits, such as flower color, odor,
shape, inflorescence architecture and the types and quantities of
the floral rewards, on the primary functions of the flowers: the
attraction of pollinators and the dispersal of pollen from the
anthers and the deposition of pollen onto the stigma (e.g.
Darwin, 1862). However, floral ecologists quickly learned that
unwanted animal visitors, such as those that steal the nectar
without affecting pollination and those that eat flowers, can have
adverse effects on pollinator attraction and the number and quality of the offspring that are produced by plants through both the
male (pollen) and female (seed production) roles. Moreover,
these unwanted visitors are thought to have had a profound influence on the evolution of floral traits (e.g. Inouye, 1983; Strauss
et al., 1996). For example, tubular flowers typically protect their
nectar at the base of the tube with thick leathery calyces that
cannot be easily punctured or chewed by nectar robbers. More
recently, some floral volatiles have been shown to function as
deterrents against flower feeding by herbivorous insects (e.g.
Junker & Bluethgen, 2008; Kessler et al., 2008; Willmer et al.,
2009). The study by Huang et al. suggests that the bouquet of a
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floral fragrance can also be influenced by pathogens. Clearly,
floral traits evolve under a complex set of selective pressures: they
must attract and reward pollinators for the proper dissemination
of pollen to conspecifics and the proper deposition of pollen from
conspecifics but they must also discourage unwanted floral visitors, including pathogenic microbes, or suffer the adverse fitness
consequences of these visitors.
Do other floral traits function in pathogen
resistance?
It is reasonable to expect that floral exposure to microbial pathogens would increase with time and the number and types of
animal visitors. The longevity of unpollinated flowers ranges
from a few hours in Datura spp., Cucurbita spp. and many other
species to several weeks in some orchid species (Primack, 1985).
Shykoff et al. (1996) noted that in natural populations of two
species of dioecious Silene, the male plants had both longer
floral lifetimes and a higher incidence of the pollinator vectored fungal disease, Microbotrium violaceum, than the female
plants. They proposed that differences in the infection rate
between the two sexes could be due to differences in floral longevity and later demonstrated that male and female plants
differ in risk of infection per contact (Kaltz & Shykoff, 2001).
These studies suggest that floral longevity may represent a
tradeoff between expected fitness payoffs (additional pollen
donation and pollen accumulation on the stigma) and the risk
of pathogen infection.
In virtually all species, including the long-lived flowers of orchids, pollination, the entry of pollen tubes into the ovary or
fertilization, is associated with a rapid senescence of the styles and
other floral organs (e.g. Stead, 1992). In maize, the spores of
several species of ear rot fungi are transported to the silks (styles)
by air currents and by silk feeding corn root worm beetles. The
fungal spores germinate and grow through the silks and infect
the parent plant and its seeds. Maize silks rapidly collapse and
senesce when pollen tubes enter into the ovary from the silks.
During an unusually cool and wet summer that was ideal for the
proliferation of ear rot fungi, Valdivia et al. (2006) showed under
field conditions that a 12-h post-pollination delay in the senescence of silks resulted in a nearly three-fold increase (72% vs
25%) in the incidence of ear rot fungi in the resulting ears,
suggesting that rapid style senescence may function in pathogen
resistance.
Because nectar is composed primarily of simple sugars, it is a
rich media for the growth of microbes and the nectars of many
species are known to contain anti-microbial chemicals and proteins (Nicolson & Thornburg, 2007; Hillwig et al., 2010).
Moreover, the nectary provides a relatively easy route for pathogen invasion into the vascular system of plants and several
pathogens are known to enter plants via the nectaries of flowers
(see Sasu et al., 2010a). In wild and cultivated squash (Cucurbita
pepo) and other cultivated cucurbits, Erwinia tracheiphila, the
causative agent of bacterial wilt disease, is transmitted by cucumber beetles (Fig. 1). The beetles acquire the pathogen when they
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Fig. 1 Cucumber beetles aggregate in the flowers of wild squash
(Cucurbita pepo ssp. texana) to feed and mate. When their frass
containing the bacterium Erwinia tracheiphila falls onto the nectary, this
deadly pathogen enters the plant via the nectary. Removal of the antimicrobial nectar by bees facilitates the entry of the pathogen. Photo
courtesy of M. A. Sasu.
feed on infected leaves and they transmit the pathogen in wild
squash when they aggregate in the flowers of nearby plants to
mate and their infected frass falls onto or near the nectary (Sasu
et al., 2010a). Sasu et al. (2010b) showed that the nectar of wild
squash is strongly antibiotic and inhibits the growth of
E. tracheiphila in vitro as effectively as 5% ampicillin for 12 h
and, in vivo, it dramatically reduces probability of infection.
Interestingly, the flowers of both cultivated and wild C. pepo are
only open for 5–6 h on one morning and they abscise 24–36 h
after anthesis. Consequently, E. tracheiphila must traverse the
nectary, enter the vascular system and move below the abscission
zone within 24 h if infection is to occur. Consequently, the antibiotic nectar merely needs to retard the growth of E. tracheiphila
in order to be effective.
Although floral ecologists are just beginning to look at the roles
of floral traits in pathogen resistance, it is already apparent that a
given floral trait is likely to play multiple roles. For example, pollinators associate the fragrance of a flower with nectar and pollen
rewards but individual components in the bouquet may also serve
to discourage floral herbivores and resist disease transmission. As
noted by Huang et al., many anti-pathogen defenses, including
defensive volatile compounds, evolved before flowering plants,
and consequently, their roles in pollination (pollinator attraction
and pollen dispersal) may be secondary and derived. In this regard,
flavonols, many of which are known to have anti-microbial properties, accumulate on the stigmas of many species in response to
pollination and damage to floral organs and have been shown to
play a role in pollen germination and tube growth (Taylor &
Hepler, 1997), but their role in floral pathogen resistance has not
been explored. It is also worthwhile to note that sporophytic selfincompatibility in the Brassicaceae has strong similarities to antifungal defenses (Dickinson, 1994) while the Solanaceous-type of
gametophytic self-incompatibility has strong homologies to
RNase based bacterial and virus defenses (Hillwig et al., 2010).
Pollination is risky to both the parent plant and its offspring …
2012 The Author
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Phytologist
Commentary
and floral ecologists are discovering that prudent plants possess
traits that allow them to practice safe sex.
Andrew G. Stephenson
Department of Biology, 208 Mueller Laboratory, The
Pennsylvania State University, University Park, PA 16802, USA
(tel +1 814 863 1553; email [email protected])
References
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Dickinson HG. 1994. Simply a social disease? Nature 367: 517–518.
Hillwig MS, Liu X, Liu G, Thornburg RW, MacIntosh GC. 2010. Petunia
nectar proteins have ribonuclease activity. Journal of Experimental Botany 61:
2951–2965.
Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J,
Tholl D. 2012. The major volatile organic compound emitted from
Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense
against a bacterial pathogen. New Phytologist 193: 997–1008.
Inouye DW. 1983. The ecology of nectar robbing. In: Bentley B, Elias T, eds.
Biology of nectaries. New York, NY, USA: Columbia University Press, 153–173.
Junker RR, Bluethgen N. 2008. Floral scents repel potentially nectar-thieving
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contact risk of infection by sexually transmitted disease. Journal of Ecology 89:
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Kessler D, Gase K, Baldwin IT. 2008. Field experiments with transformed plants
reveal the sense of floral scents. Science 321: 1200–1202.
Nicolson SW, Thornburg RW. 2007. Nectar chemistry. In: Nicolson SW, Nepi
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Primack RB. 1985. Longevity of individual flowers. Annual Review of Ecology and
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Sasu MA, Seidl-Adams I, Wall K, Winsor JA, Stephenson AG. 2010a. Floral
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Shykoff JA, Bucheli E, Kaltz O. 1996. Flower lifespan and disease risk. Nature
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Stead AD. 1992. Pollination induced flower senescence: a review. Plant Growth
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Strauss SY, Conner JK, Rush SL. 1996. Foliar herbivory affects floral characters
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Taylor LP, Hepler PK. 1997. Pollen germination and tube growth. Annual
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Valdivia ER, Cosgrove DJ, Stephenson AG. 2006. Role of accelerated
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Willmer PG, Nuttman CV, Raine NE, Stone GN, Pattrick JG, Henson K,
Stillman P, McIlroy L, Potts SG, Knudsen JT. 2009. Floral volatiles
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Key words: anti-microbial nectar, (E)-b-caryophyllene, floral traits,
pathogens, plant diseases, pollination, resistance, volatile organic compounds
(VOCs).
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