scholarly journals Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene

2020 ◽  
Vol 117 (37) ◽  
pp. 23148-23157 ◽  
Author(s):  
Cuong Nguyen Huu ◽  
Barbara Keller ◽  
Elena Conti ◽  
Christian Kappel ◽  
Michael Lenhard

Heterostyly represents a fascinating adaptation to promote outbreeding in plants that evolved multiple times independently. While l-morph individuals form flowers with long styles, short anthers, and small pollen grains, S-morph individuals have flowers with short styles, long anthers, and large pollen grains. The difference between the morphs is controlled by an S-locus “supergene” consisting of several distinct genes that determine different traits of the syndrome and are held together, because recombination between them is suppressed. In Primula, the S locus is a roughly 300-kb hemizygous region containing five predicted genes. However, with one exception, their roles remain unclear, as does the evolutionary buildup of the S locus. Here we demonstrate that the MADS-box GLOBOSA2 (GLO2) gene at the S locus determines anther position. In Primula forbesii S-morph plants, GLO2 promotes growth by cell expansion in the fused tube of petals and stamen filaments beneath the anther insertion point; by contrast, neither pollen size nor male incompatibility is affected by GLO2 activity. The paralogue GLO1, from which GLO2 arose by duplication, has maintained the ancestral B-class function in specifying petal and stamen identity, indicating that GLO2 underwent neofunctionalization, likely at the level of the encoded protein. Genetic mapping and phylogenetic analysis indicate that the duplications giving rise to the style-length-determining gene CYP734A50 and to GLO2 occurred sequentially, with the CYP734A50 duplication likely the first. Together these results provide the most detailed insight into the assembly of a plant supergene yet and have important implications for the evolution of heterostyly.

Development ◽  
1996 ◽  
Vol 122 (11) ◽  
pp. 3433-3441 ◽  
Author(s):  
M.C. Perbal ◽  
G. Haughn ◽  
H. Saedler ◽  
Z. Schwarz-Sommer

In Antirrhinum majus, petal and stamen organ identity is controlled by two MADS-box transcription factors, DEFICIENS and GLOBOSA. Mutations in either of these genes result in the replacement of petals by sepaloid organs and stamens by carpelloid organs. Somatically stable def and glo periclinal chimeras, generated by transposon excision events, were used to study the non-cell-autonomous functions of these two MADS-box proteins. Two morphologically distinct types of chimeras were analysed using genetic, morphological and molecular techniques. Restoration of DEF expression in the L1 cell layer results in the reestablishment of DEF and GLO functions in L1-derived cells only; inner layer cells retain their mutant sepaloid features. Nevertheless, this activity is sufficient to allow the expansion of petal lobes, highlighting the role of DEF in the stimulation of cell proliferation and/or cell shape and elongation when expressed in the L1 layer. Establishment of DEF or GLO expression in L2 and L3 cell layers is accompanied by the recovery of petaloid identity of the epidermal cells but it is insufficient to allow petal lobe expansion. We show by in situ immunolocalisation that the non-cell-autonomy is due to direct trafficking of DEF and GLO proteins from the inner layer to the epidermal cells. At least for DEF, this movement appears to be polar since DEF acts cell-autonomously when expressed in the L1 cell layer. Furthermore, the petaloid revertant sectors observed on second whorl mutant organs and the mutant margins of petals of L2L3 chimeras suggest that DEF and GLO intradermal movement is limited. This restriction may reflect the difference in the regulation of primary plasmodesmata connecting cells from the same layer and secondary plasmodesmata connecting cells from different layers. We propose that control of intradermal trafficking of DEF and GLO could play a role in maintaining of the boundaries of their expression domains.


2020 ◽  
Author(s):  
Chunling Zhang ◽  
Yalin Sun ◽  
Ludan Wei ◽  
Wenjing Wang ◽  
Hang Li ◽  
...  

Abstract Background: Members of AP1/FUL subfamily genes play an essential role in the regulation of floral meristem transition, floral organ identity, and fruit ripping. At present, there have been insufficient studies to explain the function of the AP1/FUL-like subfamily genes in Asteraceae. Results: Here, we cloned two euAP1 clade genes TeAP1-1 and TeAP1-2, and three euFUL clade genes TeFUL1, TeFUL2, and TeFUL3 from marigold (Tagetes erecta). Expression profile analysis demonstrated that TeAP1-1 and TeAP1-2 were mainly expressed in receptacles, sepals, petals, and ovules. TeFUL1 and TeFUL3 were expressed in floral buds, stems and leaves as well as in productive tissues, while TeFUL2 was mainly expressed in floral buds and vegetative tissues. Transgenic Arabidopsis lines showed that overexpression TeAP1-2 or TeFUL2 resulted in early flowering, implying that these two genes might regulate the floral transition. Yeast two-hybrid analysis indicated that TeAP1/FUL proteins only interacted with TeSEP proteins to form heterodimers, and that TeFUL2 could also form a homodimer.Conclusion: In general, TeAP1-1 and TeAP1-2 might play a conserved role in regulating sepal and petal identity, just like the role of MADS-box class A genes, while TeFUL genes might display divergent functions. This study provides an insight into molecular mechanism of AP1/FUL-like genes in Asteraceae species.


2006 ◽  
Vol 6 ◽  
pp. 1933-1944 ◽  
Author(s):  
Wen-Chieh Tsai ◽  
Hong-Hwa Chen

Orchids are known for both their floral diversity and ecological strategies. The versatility and specialization in orchid floral morphology, structure, and physiological properties have fascinated botanists for centuries. In floral studies, MADS-box genes contributing to the now famous ABCDE model of floral organ identity control have dominated conceptual thinking. The sophisticated orchid floral organization offers an opportunity to discover new variant genes and different levels of complexity to the ABCDE model. Recently, several remarkable research studies done on orchid MADS-box genes have revealed the important roles on orchid floral development. Knowledge about MADS-box genes’' encoding ABCDE functions in orchids will give insights into the highly evolved floral morphogenetic networks of orchids.


Plants ◽  
2020 ◽  
Vol 9 (12) ◽  
pp. 1767
Author(s):  
Annemarie Heiduk ◽  
Dewi Pramanik ◽  
Marlies Spaans ◽  
Loes Gast ◽  
Nemi Dorst ◽  
...  

Deceptive Ceropegia pitfall flowers are an outstanding example of synorganized morphological complexity. Floral organs functionally synergise to trap fly-pollinators inside the fused corolla. Successful pollination requires precise positioning of flies headfirst into cavities at the gynostegium. These cavities are formed by the corona, a specialized organ of corolline and/or staminal origin. The interplay of floral organs to achieve pollination is well studied but their evolutionary origin is still unclear. We aimed to obtain more insight in the homology of the corona and therefore investigated floral anatomy, ontogeny, vascularization, and differential MADS-box gene expression in Ceropegia sandersonii using X-ray microtomography, Light and Scanning Electronic Microscopy, and RT-PCR. During 10 defined developmental phases, the corona appears in phase 7 at the base of the stamens and was not found to be vascularized. A floral reference transcriptome was generated and 14 MADS-box gene homologs, representing all major MADS-box gene classes, were identified. B- and C-class gene expression was found in mature coronas. Our results indicate staminal origin of the corona, and we propose a first ABCDE-model for floral organ identity in Ceropegia to lay the foundation for a better understanding of the molecular background of pitfall flower evolution in Apocynaceae.


1996 ◽  
Vol 10 (4) ◽  
pp. 663-677 ◽  
Author(s):  
Brendan Davies ◽  
Alexandra Rosa ◽  
Tinka Eneva ◽  
Heinz Saedler ◽  
Hans Sommer

2012 ◽  
Vol 160 (2) ◽  
pp. 788-807 ◽  
Author(s):  
Xianchun Sang ◽  
Yunfeng Li ◽  
Zengke Luo ◽  
Deyong Ren ◽  
Likui Fang ◽  
...  

2017 ◽  
Vol 8 ◽  
Author(s):  
Yingjun Chi ◽  
Tingting Wang ◽  
Guangli Xu ◽  
Hui Yang ◽  
Xuanrui Zeng ◽  
...  

2001 ◽  
Vol 48 (2) ◽  
pp. 351-358 ◽  
Author(s):  
H Saedler ◽  
A Becker ◽  
K U Winter ◽  
C Kirchner ◽  
G Theissen

MADS-box genes encode transcription factors in all eukaryotic organisms thus far studied. Plant MADS-box proteins contain a DNA-binding (M), an intervening (I), a Keratin-like (K) and a C-terminal C-domain, thus plant MADS-box proteins are of the MIKC type. In higher plants most of the well-characterized genes are involved in floral development. They control the transition from vegetative to generative growth and determine inflorescence meristem identity. They specify floral organ identity as outlined in the ABC model of floral development. Moreover, in Antirrhinum majus the MADS-box gene products DEF/GLO and PLE control cell proliferation in the developing flower bud. In this species the DEF/GLO and the SQUA proteins form a ternary complex which determines the overall "Bauplan" of the flower. Phylogenetic reconstructions of MADS-box sequences obtained from ferns, gymnosperms and higher eudicots reveal that, although ferns possess already MIKC type genes, these are not orthologous to the well characterized MADS-box genes from gymnosperms or angiosperms. Putative orthologs of floral homeotic B- and C-function genes have been identified in different gymnosperms suggesting that these genes evolved some 300-400 million years ago. Both gymnosperms and angiosperms also contain a hitherto unknown sister clade of the B-genes, which we termed Bsister. A novel hypothesis will be described suggesting that B and Bsister might be involved in sex determination of male and female reproductive organs, respectively.


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