Close, Yet Separate: Patterns of Male and Female Floral Development in Monoecious Species

Perl‐Treves, Rafael; Rajagopalan, Prem Anand

doi:10.1002/9780470988602.ch6

Cited by 9 publications

(9 citation statements)

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“…Identifying M locus as an ethylene biosynthesis gene expressed in the carpel is rather surprising. Models that predicted the action of F and M suggested that F determines threshold levels of ethylene that are required to perform a dual action: promote pistil development and inhibit stamen formation in the pistillate flowers [4] , [7] , [26] . The action of F appears to be gradual and “systemic”: femaleness increases along the shoot and can “diffuse” from an FF rootstock to an ff scion [27] .…”

Section: Discussionmentioning

confidence: 99%

“…Thus, gynoecious plants bear only pistillate flowers, androecious plants bear only staminate flowers, and monoecious plants develop a succession of male flowers, followed by female flowers. Hermaphrodites have only bisexual flowers and andromonoecious plants have both male and bisexual flowers [3] , [4] . For decades, cucumber has been the model plant for the study of plant sex determination [5] , [6] .…”

Section: Introductionmentioning

confidence: 99%

“…The sex-determining genetic program is also affected by environmental conditions and can be manipulated by exogenous hormone treatments. Moreover, endogenous hormone levels were correlated with cucumber sexual development [3] , [4] . Among the different hormones that have been implicated in cucumber sex expression, ethylene was shown to play a key-role.…”

Section: Introductionmentioning

confidence: 99%

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A Conserved Ethylene Biosynthesis Enzyme Leads to Andromonoecy in Two Cucumis Species

et al. 2009

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Andromonoecy is a widespread sexual system in angiosperms, characterized by plants carrying both male and bisexual flowers. Monoecy is characterized by the presence of both male and female flowers on the same plant. In cucumber, these sexual forms are controlled by the identity of the alleles at the M locus. In melon, we recently showed that the transition from monoecy to andromonoecy result from a mutation in 1-aminocyclopropane-1-carboxylic acid synthase (ACS) gene, CmACS-7. To isolate the andromonoecy gene in cucumber we used a candidate gene approach in combination with genetical and biochemical analysis. We demonstrated co-segregation of CsACS2, a close homolog of CmACS-7, with the M locus. Sequence analysis of CsACS2 in cucumber accessions identified four CsACS2 isoforms, three in andromonoecious and one in monoecious lines. To determine whether the andromonoecious phenotype is due to a loss of ACS enzymatic activity, we expressed the four isoforms in Escherichia coli and assayed their activity in vitro. Like in melon, the isoforms from the andromonoecious lines showed reduced to no enzymatic activity and the isoform from the monoecious line was active. Consistent with this, the mutations leading andromonoecy were clustered in the active site of the enzyme. Based on this, we concluded that active CsACS2 enzyme leads to the development of female flowers in monoecious lines, whereas a reduction of enzymatic activity yields hermaphrodite flowers. Consistent with this, CsACS2, like CmACS-7 in melon, is expressed specifically in carpel primordia of buds determined to develop carpels. Following ACS expression, inter-organ communication is likely responsible for the inhibition of stamina development. In both melon and cucumber, flower unisexuality seems to be the ancestral situation, as the majority of Cucumis species are monoecious. Thus, the ancestor gene of CmACS-7/CsACS2 likely have controlled the stamen development before speciation of Cucumis sativus (cucumber) and Cucumis melo (melon) that have diverged over 40 My ago. The isolation of the genes for andromonoecy in Cucumis species provides a molecular basis for understanding how sexual systems arise and are maintained within and between species.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Conserved Ethylene Biosynthesis Enzyme Leads to Andromonoecy in Two Cucumis Species

et al. 2009

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“…Unisexual flower development is therefore considered a mechanism for promoting cross-pollination (Barrett, 2002). Although substantial progress has been made in understanding what determines plant sex (reviewed by Ainsworth, 1999;Tanurdzic and Banks, 2004;Perl-Treves and Rajagopalan, 2006;Boualem et al, 2008Boualem et al, , 2009Li et al, 2009;Martin et al, 2009), little is known regarding what triggers the developmental decision process, and how this process is carried out in an organ-specific manner.…”

Section: Introductionmentioning

confidence: 99%

Ethylene perception is involved in female cucumber flower development

et al. 2010

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SUMMARYIt is well established that ethylene promotes female flower development in cucumber. However, little is known about how the gaseous hormone selectively affects female flowers, and what mechanism it uses. Previously, we found organ-specific DNA damage in the primordial anther of female cucumber flowers. This finding led to a hypothesis that ethylene might promote female flower development via the organ-specific induction of DNA damage in primordial anthers. In this study, we tested this hypothesis first by demonstrating ethylene induction of DNA damage via the ethylene signaling pathway using cucumber protoplasts. Then, using representative component genes of the ethylene signaling pathway as probes, we found that one of the ethylene receptors, CsETR1, was temporally and spatially downregulated in the stamens of stage-6 female cucumber flowers, especially along with the increase of the nodes. Furthermore, by constructing transgenic Arabidopsis plants with organ-specific expression of antisense CsETR1 under the control of an AP3 promoter to downregulate ETR1 expression in the stamens, we generated Arabidopsis 'female flowers', in which the abnormal stamens mimic those of female cucumber flowers. Our data suggest that ethylene perception is involved in the arrest of stamen development in female cucumber flowers through the induction of DNA damage. This opens up a novel perspective and approach to solve the half-century-long puzzle of how gaseous ethylene selectively promotes female flowers in the monoecious cucumber plant.

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“…Since the 1950s, it has been well documented that ethylene application in cucumber increased the ratio of female versus male Xowers (Reviewed by Perl-Treves 1999). Physiological analyses demonstrated that endogenous ethylene levels were higher in gynoecious lines than in androecious or monoecious lines (Reviewed by Rudich 1990;Malepszy and Niemirowicz-Szczytt 1991;Perl-Treves 1999;Perl-Treves and Rajagopalan 2006). Yin and Quinn (1995) proposed that ethylene played a crucial role in regulating the sex expression in cucumber, while Kater et al (2001) proposed that the sex determination is restricted to particular whorls, rather than to their sexual identity.…”

Section: Introductionmentioning

confidence: 99%

Stamen development in Arabidopsis is arrested by organ-specific overexpression of a cucumber ethylene synthesis gene CsACO2

Duan

Wang

et al. 2008

Planta

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Cucumber (Cucumis sativus L.) has served as a model to understand hormone regulation in unisexual flower development since the 1950s and the role of ethylene in promoting female flower development has been well documented. Recent studies cloned the F-locus in gynoecious lines as an additional copy of the ACC synthase (ACS) gene, which further confirmed the role of ethylene in the promotion of female cucumber flowers. However, no direct evidence was generated to demonstrate that increases in endogenous ethylene production could induce female flowers by arresting stamen development. To clarify the relationship between ethylene production and stamen development, we overexpressed the ethylene synthesis cucumber gene CsACO2 to generate transgenic Arabidopsis, driven by the organ-specific promoter P ( AP3 ). We found that organ-specific overexpression of CsACO2 significantly affected stamen but not carpel development, similar to that in the female flowers of cucumber. Our results suggested that increases in ethylene production directly disturb stamen development. Additionally, our study revealed that among all floral organs, stamens respond most sensitively to exogenous ethylene.

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Close, Yet Separate: Patterns of Male and Female Floral Development in Monoecious Species

Cited by 9 publications

References 81 publications

A Conserved Ethylene Biosynthesis Enzyme Leads to Andromonoecy in Two Cucumis Species

A Conserved Ethylene Biosynthesis Enzyme Leads to Andromonoecy in Two Cucumis Species

Ethylene perception is involved in female cucumber flower development

Stamen development in Arabidopsis is arrested by organ-specific overexpression of a cucumber ethylene synthesis gene CsACO2

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