Abstract
Sex determination evolved to control the development of unisexual flowers. In agriculture, it conditions how plants are cultivated and bred. We investigated how female flowers develop in monoecious cucurbits. We discovered in melon, Cucumis melo, a mechanism in which ethylene produced in the carpel is perceived in the stamen primordia through spatially differentially expressed ethylene receptors. Subsequently, the CmEIN3/CmEIL1 ethylene signalling module, in stamen primordia, activates the expression of CmHB40, a transcription factor that downregulates genes required for stamen development and upregulates genes associated with organ senescence. Investigation of melon genetic biodiversity revealed a haplotype, originating in Africa, altered in EIN3/EIL1 binding to CmHB40 promoter and associated with bisexual flower development. In contrast to other bisexual mutants in cucurbits, CmHB40 mutations do not alter fruit shape. By disentangling fruit shape and sex-determination pathways, our work opens up new avenues in plant breeding.
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Data availability
The raw NGS data used and generated in this study have been deposited in the SRA database under accession numbers PRJNA917526, PRJNA917594 and PRJNA917630. The Charmono melon genome is publicly accessible at http://cucurbitgenomics.org/v2/ftp/genome/melon/Charmono/. All other data are available in the main text or Supplementary Tables. The described biological material can be obtained from A. Bendahmane under a material transfer agreement with INRAE.
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Acknowledgements
We thank P. Audigier, F. Vion and H. Ornstrup for taking care of the plant and the research facilities provided by the Institute of Plant Science Paris-Saclay (IPS2, France). We thank the Center of Biological Resources CRBLeg of GAFL Avignon for maintaining, characterizing and providing melon genetic resources; and the experimental unit UE AHM of Avignon for their technical expertise. This work was funded by the following: European Research Council, grant ERC-SEXYPARTH, 341076 (to A. Bendahmane); Agence Nationale de la Recherche, grant EPISEX, ANR-17-CE20-0019 (to A. Bendahmane); Agence Nationale de la Recherche, grant NECTAR, ANR-19-CE20-0023 (to A. Bendahmane); Laboratoire d’Excellence Sciences des Plantes de Saclay, grant SPS, ANR-10-LABX-40-SPS (to A. Boualem and A. Bendahmane); and the Inititiative d’Excellence Paris-Saclay, grant Lidex-3P, ANR-11-IDEX-0003-02 (to A. Bendahmane).
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Contributions
C.D., A. Boualem and A. Bendahmane conceived and designed the experiments. D.R., R.S.D., N.Y.R.-G., F.A.-C., C.T., H.M., F.-Q.T., F.M., H.-Y.H., M.H., S.Z., V.R. and Y.H. performed the experiments. D.R., R.S.D., N.Y.R.-G., F.A.-C., M.V., C.P., M.B., A. Boualem and A. Bendahmane analysed the data. D.R., R.S.D., N.Y.R.-G., F.A.-C., C.T., H.M., F.-Q.T., F.M., M.V., C.P., V.R., M.B., C.D., A. Boualem and A. Bendahmane contributed materials/analysis tools. D.R., R.S.D., N.Y.R.-G., C.D., A. Boualem and A. Bendahmane wrote the original draft. R.S.D., A. Boualem and A. Bendahmane edited the paper.
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Extended data
Extended Data Fig. 1 Sexual morph of Tibish Jebel Kordofan 4.
a, In monoecious melon, most of the flowers are male, female flowers developing on the nodes of the branches. Tibish Jebel Kordofan 4 (TK4) develops hermaphrodite flowers at the position of the female flowers. sg, stigma; st, stamen. Scale bars, 1 cm. b, Protein sequence alignment of CmACS7 of CharMono and TK4. c, Expression profiling of CmACS7 in pistillate flower buds at stage 6 of CharMono and TK4. Bars represent mean ± SD (n = 4 biologically independent assays).
Extended Data Fig. 2 Sexual morphs observed in monoecious CharMono and andromonoecious TK-BC5 lines.
a, Graphic representation of flower sexual types observed in CharMono and TK-BC5 lines. b, CharMono male and female flowers. c, TK-BC5 male and hermaphrodite flowers. sg, stigma; st, stamen. Scale bars in (b) and (c), 2 mm. d, Percent of female and hermaphrodite flowers among pistillate flowers in CharMono, TK-BC5 and in the resulting F1 hybrid. Data in d are means ± s.d. from 7 independent plants. e, Segregation analysis of andromonoecious phenotype in F2 populations. Nb, total number of plants. Plants are considered monoecious (*) if they harbour male and female flowers; andromonoecious (**) if in addition to male flower, more than 50% of pistillate flowers are hermaphrodite. f, Ovary shape index in CharMono, TK-BC5 and in Cmhb-W113* and Cmacs7 loss of function mutants. Data in f are representative of 20 flowers at anthesis over 10 independent plants. P values are calculated using two-way ANOVA with Tukey’s multiple comparisons test. g, Genome-wide distribution of Δ SNP index identified between CharMono and TK4 DNA bulks. Δ SNP index is shown according to SNP position (Mb) on each chromosome. The highest Δ SNP index, red arrowhead, found on chromosome 8, was confirmed to correspond to the M2 mutation.
Extended Data Fig. 3 Sexual morph and ovary shape phenotypes observed in wild type cucumber and Cshb40W113* TILLING mutant and CsHB40 expression pattern.
a, Schematic of the sexual morphs of wild-type monoecious cucumber line Poinsett 76 and Cshb40W113* TILLING mutant. In wild-type monoecious cucumber, flowers develop following a defined sequence along the main stem with 5 nodes carrying male flowers and the 6th node carrying a female flower. Female flowers were transformed into hermaphrodite flowers in Cshb40W113* TILLING mutant. b, Graphic presentation of flower sexual types observed in monoecious cucumber and Cshb40W113* mutant. Each column represents an individual plant and each rectangle represents a node. Flower sex types are shown for at least 20 nodes. Cshb40Q107* has identical sexual morph as Cshb40W113* mutant. c, Male and female flowers from wild-type monoecious cucumber. d, Male and hermaphrodite flowers from Cshb40W113* mutant. sg, stigma; st, stamen. Scale bars in (c) and (d), 2 mm. e, Ovary shape index in wild type Poinsett 76, in Cshb40W113* and Csacs7G33C loss of function mutants. Data in e are representative of 25 flowers at anthesis over 15 independent plants. P values are calculated using two-way ANOVA with Tukey’s multiple comparisons test. f–h, CsHB40 in situ expression in flower buds of cucumber at stage 6. f, Wild-type female flower; g, Hermaphrodite flower from Csacs2 mutant; h, Wild-type male flower. c, carpel primordia; st, stamen primordia; p, petal; s, sepal. Scale bars, 100 µm. In situ expression analysis were performed five times on independent flowers with similar results.
Extended Data Fig. 4 Phylogenetic analysis of HD-ZIP protein family.
Phylogenic analysis of HD-ZIP proteins in Arabidopsis, cucumber and melon, inferred using Neighbour-joining method. Protein sequences were aligned and used to generate the neighbour-joining phylogenetic tree with 1,000 bootstrap replicates. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test are shown next to the branches. CmHB40 and CsHB40 correspond to MELO3C007809 in melon and Csa6G501990.1 in cucumber, respectively.
Extended Data Fig. 5 Methylation landscape and sequence diversity of CmHB40 in 456 melon accessions.
a, Genomic profile of the region surrounding CmHB40; TK-BC5 (purple), CharMono (light green) methylation profile for CpG, CHG and CHH context and CharMono ATAC-seq profile. No significant differentially methylated region was detected. b, Worldwide distribution of melon accessions used in this study. c, CmHB40 haplotype identified in melon accessions from different geographic regions. Accessions are classified in monoecious (M) and andromonoecious (AM) and whether they harbour wild-type CmACS7 or Cmacs7A57V allele. H1, haplotype 1.
Extended Data Fig. 6 Positional cloning of M3 and M4 mutations.
a, M3 and M4 are not altered in CmACS7 protein sequence. b, Segregation analysis of andromonoecious phenotype in M3 and M4 F2 backcross populations. Nb, total number of plants. c, Genome-wide distribution of Δ SNP index identified in bulk DNA of CharMono and M3 F2 segregant plants. d, Δ SNP index identified in bulk DNA of CharMono and M4 F2 segregant plants. The highest Δ SNP index, arrowhead, found on chromosome 2 and chromosome 3 were confirmed to correspond to the M3 and the M4 mutations, respectively. Δ SNP index is shown according to SNP position (Mb) on each chromosome. e, Phylogenic analysis of CmEIN3 related proteins in melon and Arabidopsis. Protein sequences were aligned and used to generate the neighbour-joining phylogenetic tree with 1,000 bootstrap replicates. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test are shown next to the branches.
Extended Data Fig. 7 Analysis of ein3 and eil1 mutants.
a, The triple response phenotypes of ein3 and eil1 mutants. Seedlings were germinated in the dark on water- soaked paper in presence or not of 6 μM Ethephon. Scale bars, 3 cm. b, qRT–PCR analysis of CmEIN3 and CmEIL1 in leaf, stem and flower buds collected at stage 6. c, Table showing the effect of CmEIN3 and CmEIL1 allelic combinations on the sex of the plant. d, Stamen size observed in the EIN3 and EIL1 allelic combinations. Scale bars, 2 mm. e, Frequency of short, medium and normal stamina in ein3 and eil1 single and double mutants. The double-mutant display mainly normal stamina as the one observed in hermaphrodite flowers. f, Sexual morph and fruit shape phenotypes of gynoecious melon (wip1 mutant) and hermaphrodite wip1ein3 eil1 triple mutant. Scale bars, 5 mm. g,h, Melon ovary shape index of ein3 and eil1 mutant flowers in the monoecious (g) and gynoecious (h) genetic backgrounds. i, qRT–PCR analysis of CmWIP1 in flower buds collected at stage 6 in wild-type, hb40, ein3 and eil1 mutant lines. Data in b and i are means ± s.d. from 6 biological replicates. P values are calculated using using one-way ANOVA with Tukey’s multiple comparisons test. Data in e are means ± s.d. representative of 40 flowers at anthesis over 4 independent plants. Data in g and h are representative of at least 13 flowers at anthesis over 10 independent plants. P values are calculated using two-way ANOVA with Tukey’s multiple comparisons test.
Extended Data Fig. 8 Sequence alignment and conservation of EBS1 in CmHB40 promoter.
a, Sequence alignment of CharMono and TK4 genomic DNA overlapping EIN3/EIL1 binding Site. EIN3/EIL1 binding site sequences of EBS1 are highlighted in red. The deletion of 460 bp in TK4 genome and associated with the andromonoecy is shown. b, 70%~Sequence Conservation analysis of CmHB40 promoter in monoecious cucurbit species. mVISTA plot of CmHB40 promoter and coding regions orthologs in monoecious cucurbit species. The height of the plot on the y-axis indicates the percentage of nucleotide identity (50%–100%). Pink and white peaks indicate conserved nucleotide sequences (CNSs) with identity >70% and 50% within 100 base pairs, respectively. Red line indicates the location of CmEIN3 binding motif validated using EMSA. Dashed box indicates the Δ460 deletion in the promoter of TK4 genome. ATAC-Seq was used to identify open chromatin region (See Fig. 3). c, d, CmEIL1 binds to EBS1 in the CmHB40 promoter. c, EMSA assay. A 5-μM GST or EIL1-GST protein and a 10-nM DNA probe were used. P1-m1 to P1-m3, mutant probes. GST, Glutathione S-transferase. EMSA assay was performed three times with similar results. d, ChIP–qPCR assay in melon protoplast transformed with 35 S:EIL1-GFP. Results are expressed as a percentage of the Input fraction. Wild-type protoplasts were used as negative controls. Data in d are means ± s.d. from 3 biological replicates. P values are calculated using two-tailed Student’s t-test.
Extended Data Fig. 9 Gene expression profiling of stamen primordia of female, male and Cmhb40W113* and acs7A57V hermaphrodites flowers.
a, Venn diagram showing overlap between the pairwise comparison groups. R-Factor, the representation factor is the number of overlapping genes divided by the expected number of overlapping genes drawn from two independent groups. A representation factor > 1 indicates more overlap than expected of two independent groups. One-sided Fisher’s exact test P values are indicated. b, GO term enriched among the 387 common DEGs. Adjusted P value were calculated using one-sided Fisher’s exact test. c, LCM-seq heat maps of ethylene-, auxin- and gibberellin-related genes differentially expressed in stamen primordia of female, hermaphrodites and male flowers.
Extended Data Fig. 10 Analysis of etr1 and etr2 mutants.
a, Phylogenic analysis of ethylene receptors in melon and Arabidopsis. Protein sequences were aligned and used to generate the neighbour-joining phylogenetic tree with 1,000 bootstrap replicates. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test are shown next to the branches. b, qRT–PCR analysis of CmEIN3 and CmEIL1 in leaf, stem and flower buds collected at stage 6. c–e, qRT–PCR of CmERS1, CmEIN3 and CmEIL1 in LCM carpel and stamen primordia of female, hermaphrodite and male flowers. f, Sexual morphs observed in Cmetr1P253S and Cmetr2W530* TILLING mutants. Hermaphrodite flowers of Cmetr1P253S mutants showed wide variation in the size of stamens. Whereas, Cmetr2W530* mutant did not bear any hermaphrodite flowers. Scale bar, 5 mm. g, Graph showing the proportion of hermaphrodite and female flowers in monoecious melon (Wild-type), homozygous Cmetr1P253S mutant (etr1/etr1) and heterozygous Cmetr1P253S mutant (etr1/ETR1). h, At left, an adult melon WT control plant. In the middle, an adult plant homozygous for the mutation Cmetr1P253S (etr1/etr1) and heterozygous for the mutation Cmetr2W530* (ETR2/etr2) with stunted vegetative growth and complete inhibition in the florescence. At right, an adult melon plant homozygous for Cmetr1P253S and has WT ETR2 alleles. Scale bar, 15 cm. Data in b are means ± s.d. from 6 biological replicates. P values are calculated using using one- way ANOVA with Tukey’s multiple comparisons test. Data in c to e are means ± s.d. from 3 biological LCM replicates. P values are calculated using two-tailed Student’s t-test.
Supplementary information
Supplementary Tables
Supplementary Table 1: List of TILLING mutants generated in this study. Table 2: Origins, sexual phenotypes and CmHB40 haplotypes of all C. melo accessions used in this study. Table 3: Differentially expressed genes in stamen primordia of hb40W113* and acs7A57V hermaphrodite flowers and male flowers. The RNA expression data were normalized to the value in stamen primordia of female flowers. Table 4: Primers used in this study.
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Rashid, D., Devani, R.S., Rodriguez-Granados, N.Y. et al. Ethylene produced in carpel primordia controls CmHB40 expression to inhibit stamen development. Nat. Plants 9, 1675–1687 (2023). https://doi.org/10.1038/s41477-023-01511-z
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DOI: https://doi.org/10.1038/s41477-023-01511-z
