A single gene underlies the dynamic evolution of poplar sex determination

Müller, Niels A.; Kersten, Birgit; Montalvão, Ana Paula Leite; Mähler, Niklas; Bernhardsson, Carolina; Bräutigam, Katharina; Lorenzo, Zulema Carracedo; Hoenicka, Hans; Kumar, Vikash; Mäder, Malte; Pakull, Birte; Robinson, Kathryn M.; Sabatti, Maurizio; Vettori, Cristina; Ingvarsson, Pär K.; Cronk, Quentin; Street, Nathaniel R.; Fladung, Matthias

doi:10.1038/s41477-020-0672-9

Cited by 179 publications

(293 citation statements)

References 80 publications

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“…Aligning the sequences flanking P. davidiana's YHS to P. deltoides and P. trichocarpa genomes revealed that this YHS is in the pericentromeric region of chromosome XIX. The different locations in species in the two subgenera support the hypothesis that their dioecy evolved independently 29 , yet involved a similar mechanism.…”

Section: Resultssupporting

confidence: 57%

“…We named the FERR duplicate FERR-R, standing for its inferred FERR repressor function, as deduced from experiments described below. A duplication of FERR was also recently found in the P. tremula sex-determining region (which is located in a different chromosome XIX region from that of P. deltoides), and was named ARR17 inverted repeat 29 . EVM0039005 (also within YHS1) was found to produce long non-coding transcripts (see details below), and was named MSL, for male-specific lncRNA.…”

Section: Resultsmentioning

confidence: 88%

“…FERR-like genes resembling A. thaliana ARR17 were among candidate sex determining genes in several previous studies of poplar and willow species (PbRR9 in P. balsamifera 26,37 , PtRR9 or PtRR11 in P. trichocarpa 38 , ARR17 in P. tremula 29 , RR in Salix purpurea 22 ). Phylogenetic analysis of type-A RR genes (Supplementary Fig.…”

Section: Resultsmentioning

confidence: 91%

“…RR genes have been suggested as sex determiners in other plants, including kiwifruit 8 , S. purpurea 22 and Ginkgo 47 . Finally, a recent study showed that, in P. tremula (in subgenus Leuce, like P. davidiana), knockout of the ortholog of the P. deltoides FERR gene (ARR17 in P. tremula), in female trees converted them into males, indicating that P. tremula has a single-gene sex determination system 29 .…”

Section: Discussionmentioning

confidence: 99%

“…Genetic mapping studies revealed that the locations of the sex determining gene differ in genera Populus and its sister genus Salix [19][20][21][22][23] , suggesting independently evolved sex determination within the family Salicaceae. Multiple candidate sex determining genes have emerged from genomic association studies and/or transcriptome expression analyses [24][25][26][27][28] , including a recent study in a poplar species, P. tremula that revealed a sex determining role for one of these candidates, which was named ARR17 (Arabidopsis Response Regulator 17) 29 . In the present study, in another poplar species P. deltoides, we characterize the regulation and functions of candidate sex-determining genes.…”

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confidence: 99%

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Evidences for a role of two Y-specific genes in sex determination in Populus deltoides

et al. 2020

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Almost all plants in the genus Populus are dioecious (i.e. trees are either male or female), but it is unknown whether dioecy evolved in a common ancestor or independently in different subgenera. Here, we sequence the small peritelomeric X- and Y-linked regions of P. deltoides chromosome XIX. Two genes are present only in the Y-linked region. One is a duplication of a non-Y-linked, female-specifically expressed response regulator, which produces siRNAs that block this gene’s expression, repressing femaleness. The other is an LTR/Gypsy transposable element family member, which generates long non-coding RNAs. Overexpression of this gene in A. thaliana promotes androecium development. We also find both genes in the sex-determining region of P. simonii, a different poplar subgenus, which suggests that they are both stable components of poplar sex-determining systems. By contrast, only the duplicated response regulator gene is present in the sex-linked regions of P. davidiana and P. tremula. Therefore, findings in our study suggest dioecy may have evolved independently in different poplar subgenera.

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Section: Resultssupporting

confidence: 57%

Section: Resultsmentioning

confidence: 88%

Section: Resultsmentioning

confidence: 91%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Evidences for a role of two Y-specific genes in sex determination in Populus deltoides

et al. 2020

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Development differs between independently evolved staminode whorls in the same flower

Schenk

Appleton

2023

American J of Botany

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Premise Staminodes are commonly studied in hermaphroditic flowers, in which a fraction of the androecium evolves into infertile structures, but few studies have addressed the evolution of staminodes as they occur through the loss of stamen function in carpellate flowers. Plants of Paronychia (Caryophyllaceae) are monoecious with hermaphroditic flowers with one staminodial whorl, except for the dioecious P. chartacea and P. minima. Dioecious species have carpellate flowers that evolved an additional whorl of staminodes, providing an exceptional opportunity to study a second origin of staminodes in the same flower. Methods Using scanning electron microscopy, we observed the development of carpellate and staminate flowers to determine whether the developmental pathway of the staminodes in hermaphroditic flowers was co‐opted during the evolutionary transition to unisexual flowers. Results In carpellate flowers, antesepalous staminodes initiate as sterile anthers that develop similar to functioning stamens, but arrest before full development, leaving a rudimentary anther with lateral lobes that correspond to thecae. After antesepalous staminodes arrest, alternisepalous staminodes initiate as structures that correspond with filaments, as they do in staminate and hermaphroditic flowers. Conclusions The second origin of staminodes in carpellate flowers evolved using a different developmental pathway than what had previously evolved in the alternisepalous whorl. The two androecial whorls in the same flowers are serialogous as members of the androecium, but are paralogous as staminodes on the basis of structural and developmental differences.

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Sex‐linked gene expression and the emergence of hermaphrodites in Carica papaya

Chae

Harkess

Moore

2021

American J of Botany

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Premise One evolutionary path from hermaphroditism to dioecy is via a gynodioecious intermediate. The evolution of dioecy may also coincide with the formation of sex chromosomes that possess sex‐determining loci that are physically linked in a region of suppressed recombination. Dioecious papaya (Carica papaya) has an XY chromosome system, where the presence of a Y chromosome determines maleness. However, in cultivation, papaya is gynodioecious, due to the conversion of the male Y chromosome to a hermaphroditic Yh chromosome during its domestication. Methods We investigated gene expression linked to the X, Y, and Yh chromosomes at different floral developmental stages to identify differentially expressed genes that may be involved in the sexual transition of males to hermaphrodites. Results We identified 309 sex‐biased genes found on the sex chromosomes, most of which are found in the pseudoautosomal regions. Female (XX) expression in the sex‐determining region was almost double that of X‐linked expression in males (XY) and hermaphrodites (XYh), which rules out dosage compensation for most sex‐linked genes; although, an analysis of hemizygous X‐linked loci found evidence of partial dosage compensation. Furthermore, we identified a candidate gene associated with sex determination and the transition to hermaphroditism, a homolog of the MADS‐box protein SHORT VEGETATIVE PHASE. Conclusions We identified a pattern of partial dosage compensation for hemizygous genes located in the papaya sex‐determining region. Furthermore, we propose that loss‐of‐expression of the Y‐linked SHORT VEGETATIVE PHASE homolog facilitated the transition from males to hermaphrodites in papaya.

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A single gene underlies the dynamic evolution of poplar sex determination

Cited by 179 publications

References 80 publications

Evidences for a role of two Y-specific genes in sex determination in Populus deltoides

Evidences for a role of two Y-specific genes in sex determination in Populus deltoides

Development differs between independently evolved staminode whorls in the same flower

Sex‐linked gene expression and the emergence of hermaphrodites in Carica papaya

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