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Authors: Nguyen Hoai Nguyen, Phuong Thi Bich Ho and Linh Thi Truc Le.
Plant Reproduction (2024)
Key message: This review provides a thorough and comprehensive perspective on the topic of cucumber sexual expression. Specifically, insights into sex expression mediated by pathways other than ethylene are highlighted.
Abstract: "Cucumber (Cucumis sativus L.) is a common and important commercial crop that is cultivated and consumed worldwide. Additionally, this species is commonly used as a model for investigating plant sex expression. Cucumbers exhibit a variety of floral arrangements, comprising male, female, and hermaphroditic (bisexual) flowers. Generally, cucumber plants that produce female flowers are typically preferred due to their significant impact on the overall output. Various environmental conditions, such as temperature, light quality, and photoperiod, have been also shown to influence the sex expression in this species. Multiple lines of evidence indicate that ethylene and its biosynthesis genes are crucial in regulating cucumber sex expression. Gibberellins, another well-known phytohormone, can similarly influence cucumber sex expression via an ethylene-independent route. Further studies employing the next-generation sequencing technology also visualized a deeper slice of the molecular mechanism such as the role of the cell cycle program in the cucumber sex expression. This review aims to provide an overview of the sex expression of cucumber including its underlying molecular mechanism and regulatory aspects based on recent investigations."
Authors: Yu-Lan Zhang, Li-Ying Wang, Yi Yang, Xu Zhao, Hong-Wei Zhu, Chen You, Ning Chen, Shuai-Jie Wei, Shu-Fen Li and Wu-Jun Gao.
The Plant Journal (2024)
Significance Statement: Using environmental factors such as hormones to induce sex conversion is an important approach to studying dioecy sex differentiation, which is a special character closely related to flowering, reproduction, and fruiting. In our research, exogenous GA3 can induce functional masculinization of individual spinach, and the GA-regulating pathway was established: GA-SpGAI-SpSTM-SpPI. This study provides new ideas and theoretical support for studying the sex differentiation mechanisms of spinach and other dioecious plants.
Abstract: "The sex of dioecious plants is mainly determined by genetic factors, but it can also be converted by environmental cues such as exogenous phytohormones. Gibberellic acids (GAs) are well-known inducers of flowering and sexual development, yet the pathway of gibberellin-induced sex conversion in dioecious spinach (Spinacia oleracea L.) remains elusive. Based on sex detection before and after GA3 application using T11A and SSR19 molecular markers, we confirmed and elevated the masculinization effect of GA on a single female plant through exogenous applications of GA3, showing complete conversion and functional stamens. Silencing of GIBBERELLIC ACID INSENSITIVE (SpGAI), a single DELLA family protein that is a central GA signaling repressor, results in similar masculinization. We also show that SpGAI can physically interact with the spinach KNOX transcription factor SHOOT MERISTEMLESS (SpSTM), which is a homolog of the flower meristem identity regulator STM in Arabidopsis. The silencing of SpSTM also masculinized female flowers in spinach. Furthermore, SpSTM could directly bind the intron of SpPI to repress SpPI expression in developing female flowers. Overall, our results suggest that GA induces a female masculinization process through the SpGAI-SpSTM-SpPI regulatory module in spinach. These insights may help to clarify the molecular mechanism underlying the sex conversion system in dioecious plants while also elucidating the physiological basis for the generation of unisexual flowers so as to establish dioecy in plants."
Authors: Cristina Guerrero-Méndez and María Jazmín Abraham-Juárez
Plant Reproduction (2024)
Abstract: "Plant architecture is an important feature for agronomic performance in crops. In maize, which is a monoecious plant, separation of floral organs to produce specific gametes has been studied from different perspectives including genetic, biochemical and physiological. Maize mutants affected in floral organ development have been key to identifying genes, hormones and other factors like miRNAs important for sex determination. In this review, we describe floral organ formation in maize, representative mutants and genes identified with a function in establishing sexual identity either classified as feminizing or masculinizing, and its relationship with hormones associated with sexual organ identity as jasmonic acid, brassinosteroid and gibberellin. Finally, we discuss the challenges and scopes of future research in maize sex determination."
Authors: Satoko Nonaka, Maki Ito and Hiroshi Ezura.
Frontiers in Genome Editing (2023)
Abstract: "The gaseous plant hormone ethylene is a regulator of fruit shelf-life, one of the essential traits in fruits. Extending fruit shelf-life reduces food loss, thereby expected to contribute to food security. The enzyme 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) is the final step of the ethylene production pathway. Its suppression via antisense technology has been demonstrated to extend the shelf-life of melon, apple, and papaya. Genome editing technology is an innovative technique for plant breeding. Because the genome editing technology would not leave the exogenous genes in the final crop products, the crops via genome editing can be considered non-genetically modified yields; compared to conventional breeding, such as mutation breeding, the breeding term would be expected to be relatively short. These points include the advantage of this technique in utilization for commercial applications. We attempted to extend the shelf-life of the Japanese luxury melon (Cucumis melo var. reticulatus, ‘Harukei-3’) via modification of the ethylene synthesis pathway with the genome editing technology, CRISPR/Cas9 system. The Melonet-DB (https://melonet-db.dna.affrc.go.jp/ap/top) showed that the melon genome had the five CmACOs and the gene CmACO1 predominantly expressed in harvested fruits. From this information, CmACO1 was expected to be a key gene for shelf-life in melons. Based on this information, the CmACO1 was selected as the target of the CRISPR/Cas9 system and introduced the mutation. The final product of this melon did not have any exogenous genes. The mutation was inherited for at least two generations. In the T2 generation, the fruit phenotypes 14 days after harvest were as follows: ethylene production was reduced to one-tenth that of the wild type, pericarp colour remained green, and higher fruit firmness. Early fermentation of the fresh fruit was observed in the wild-type fruit but not in the mutant. These results show that CmACO1 knockout via CRISPR/Cas9 extended the melon’s shelf-life. Moreover, our results suggest that genome editing technology would reduce food loss and contribute to food security."
Authors: Zhongyuan Wang, Siyu Zhang, Yongchao Yang, Zheng Li, Hao Li, Rong Yu, Feishi Luan, Xian Zhang and Chunhua Wei.
Journal of Food Chemistry and Agriculture (2022)
Abstract: "The sex-control system involves several mechanisms in melon. The present study identified a novel bisexual flower control gene from the hermaphroditic melon germplasm, different from the previously recognized one. Genetic analysis showed that a single recessive gene in the newly identified locus b controlled the bisexual flower phenotype in melons. We generated 1431 F2 segregating individuals for genetic mapping of locus b, which was delimited to a 47.94 kb region. Six candidate genes were identified in the delimited interval, and candidate No. 4 encoding melon CPR5 protein was selected as the suitable one for locus b and was denoted CmCPR5. CPR5 reportedly interacted with ethylene receptor ETR1 to regulate ethylene signal transduction. Moreover, the ethephon assays showed that the parental lines (unisexual line and bisexual line) had contrasting expression patterns of CmCPR5. The BiFC and LCI assays also confirmed that CmCPR5 interacted with CmETR1 in 0426 but not in Y101. However, crossover tests showed that CmETR1 functioned normally in both parental lines, suggesting CPR5 malfunction in Y101. This study proposed a corollary mechanism of bisexual flower regulation during stamen primordium development in which the inhibition of stamen primordia development was prevented by the malfunctioning CmCPR5, resulting in bisexual flowers.
Authors: Siqi Zhang, Feng-Quan Tan, Ching-Hui Chung, Filip Slavkovic, Ravi Sureshbhai Devani, Christelle Troadec, Fabien Marcel, Halima Morin, Céline Camps, Maria Victoria Gomez Roldan, Moussa Benhamed, Catherine Dogimont, Adnane Boualem and Abdelhafid Bendahmane.
Science (2022)
One-sentence summary: In melon and cucumber plants, sex determination genes manipulate the flower meristem to develop male or female unisexual flowers.
Abstract: "Male and female unisexual flowers evolved from hermaphroditic ancestors, and control of flower sex is useful for plant breeding. We isolated a female-to-male sex transition mutant in melon and identified the causal gene as the carpel identity gene CRABS CLAW (CRC). We show that the master regulator of sex determination in cucurbits, the transcription factor WIP1 whose expression orchestrates male flower development, recruits the corepressor TOPLESS to the CRC promoter to suppress its expression through histone deacetylation. Impairing TOPLESS-WIP1 physical interaction leads to CRC expression, carpel determination, and consequently the expression of the stamina inhibitor, the aminocyclopropane-1-carboxylic acid synthase 7 (CmACS7), leading to female flower development. Our findings suggest that sex genes evolved to interfere with flower meristematic function, leading to unisexual flower development."
Authors: Jiakun Zheng and Rui Xia.
Fruit Research (2022
Abstract: "Horticultural crops are extremely valuable due to their high nutritional value, and fruits, in particular, provide indispensable vitamins and minerals. Fruit yield of edible crops is closely related to the number of flowers, which are often unisexual. The mechanism of sex differentiation in plants with unisexuality is complex, and research investigating this mechanism is in great demand. Sex determinants were first discovered in Cucurbitaceae (e.g., cucumber, melon, watermelon), and in recent years, with the rapid development of deep sequencing technologies and genomics, they have also been deciphered in some dioecious plants (e.g., persimmon, kiwifruit, asparagus). This has deepened our understanding of the evolution and diversification of sexual reproductive systems. This review summarizes recent research investigating flower sex-determination genes and their working networks, focusing on horticultural crops. Perspectives on future research in flower sex differentiation are also discussed.
Authors: Qingfei Li, Weili Guo, Bihua Chen, Feifei Pan, Helian Yang, Junguo Zhou, Guangyin Wang and Xinzheng Li.
Frontiers in Plant Science (2021)
Abstract: "The number and proportion of female flowers per plant can directly influence the yield and economic benefits of cucurbit crops. Ethephon is often used to induce female flowers in cucurbits. However, the mechanism through which it affects floral sex differentiation in pumpkin is unknown. We found that the application of ethephon on shoot apical meristem of pumpkin at seedling stage significantly increased the number of female flowers and expedited the appearance of the first female flower. These effects were further investigated by transcriptome and hormone analyses of plants sprayed with ethephon. A total of 647 differentially expressed genes (DEGs) were identified, among which 522 were upregulated and 125 were downregulated. Gene ontology (GO) and Kyoto encyclopedia of genes and genomes (KEGG) analysis indicated that these genes were mainly enriched in plant hormone signal transduction and 1-aminocyclopropane-1-carboxylate oxidase (ACO). The results suggests that ethylene is a trigger for multiple hormone signaling, with approximately 4.2% of the identified DEGs involved in ethylene synthesis and multiple hormone signaling. Moreover, ethephon significantly reduced the levels of jasmonic acid (JA), jasmonoyl-L-isoleucine (JA-ILE), and para-topolin riboside (pTR) but increased the levels of 3-indoleacetamide (IAM). Although the level of 1-aminocyclopropanecarboxylic acid was not changed, the expression of ACO genes, which code for the enzyme catalyzing the key rate-limiting step in ethylene production, was significantly upregulated after ethephon treatment. The results indicate that the ethephon affects the transcription of ethylene synthesis and signaling genes, and other hormone signaling genes, especially auxin responsive genes, and modulates the levels of auxin, jasmonic acid, and cytokinin (CK), which may together contribute to femaleness."
Authors: Yaqi Zhang, Junjun Shen, Ezra S. Bartholomew, Mingming Dong, Shuying Chen, Shuai Yin, Xuling Zhai, Zhongxuan Feng, Huazhong Ren and Xingwang Liu.
The Plant Journal (2021)
Abstract: "The fruit trichomes of Cucurbitaceae are considered the market preference among many Asian countries and have been a key determinant of cucumber cultivar selection for commercial production and breeding. However, our understanding of the initiation and development processes of cucumber trichomes is still limited. Here, we found that the cucumber TINY BRANCHED HAIR (TBH) gene was preferentially expressed in multicellular trichomes. Overexpressing CsTBH in tbh mutants restored the trichome phenotype and increased the percentage of female flowers, whereas silencing CsTBH in wild‐type plants resulted in stunted trichomes with a lower rate of female flowers. Furthermore, we provided evidence that CsTBH can directly bind to the promoters of cucumber 1‐Aminocyclopropane‐1‐Carboxylate Synthase (CsACS) genes and regulate their expression, which affects multicellular trichome development, ethylene accumulation and sex expression. Two cucumber acs mutants with different trichome morphology and sex morphs compared with their near‐isogenic line further supports our findings. Collectively, our study provides new information on the molecular mechanism of CsTBH in regulating multicellular trichome development and sex expression through an ethylene pathway."
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Authors: Mingli Liao, Zhenyong Chen, Yichao Wu, Qian Yang, Jian Zou, Zhengsong Peng, Yuhao Li, Wenxuan Liu, Zaijun Yang and Yonghong Zhou.
Journal of Plant Growth Regulation (2024)
Abstract: "Previous studies have shown that ethylene levels in flower buds are key to sex determination in plants. However, the roles of ethylene in wheat flower development are poorly understood. In this study, pistillody wheat HTS-1 (three-pistil trait), CM28TP (three-pistil trait), CS (one-pistil trait), and CM28 (one-pistil trait) were used as experimental materials. The effect of exogenous ethephon (ETH) and 1-methylcyclopropene (1-MCP) on the morphology of wheat flowers and candidate genes in the ethylene signaling pathway was investigated. The results revealed that exogenous ETH or 1-MCP treatment had a strong effect on the stamens but not on the pistils of wheat. Specifically, after treatment with ETH, the stamens of CS and CM28 became significantly shorter, while in CM28TP, 71.38% of stamens were homologously transformed into pistils or pistil-like structures (pistillody). Moreover, after treatment with 1-MCP, the pistillody stamens of HTS-1 were transformed back into stamens, and the pistillody rate decreased from 73.61 to 55.25%. Furthermore, pistillody occurred in three-pistil wheat but not in one-pistil wheat, so the three-pistil trait was closely related to the occurrence of pistillody. In addition, the expression of the ethylene transduction genes TaETR1, TaCTR1, and TaEIN2 and the ethylene response gene TaERF was upregulated under pistillody. Among them, TaCTR1 presented the highest level under pistillody, being 150 times in HTS-1 and 103 times higher in CM28TP treated with ETH than in CM28TP. Moreover, the ERELEE4 cis-acting element was found upstream of the TaCTR1 gene promoter and could facilitate homologous transformation of stamens into pistils or pistil-like structures. The results lay a theoretical foundation for analyzing the effect of ethylene on wheat flower development and supply important information for wheat hybrid breeding."
Authors: Takuya Furumoto, Shohei Yamaoka, Takayuki Kohchi, Hiroyasu Motose and Taku Takahashi.
Plant and Cell Physiology (2024)
Abstract: "Thermospermine suppresses auxin-inducible xylem differentiation, whereas its structural isomer, spermine, is involved in stress responses in angiosperms. The thermospermine synthase, ACAULIS5 (ACL5), is conserved from algae to land plants, but its physiological functions remain elusive in non-vascular plants. Here, we focused on MpACL5, a gene in the liverwort Marchantia polymorpha, that rescued the dwarf phenotype of the acl5 mutant in Arabidopsis. In the Mpacl5 mutants generated by genome editing, severe growth retardation was observed in the vegetative organ, thallus, and the sexual reproductive organ, gametangiophore. The mutant gametangiophores exhibited remarkable morphological defects such as short stalks, fasciation, and indeterminate growth. Two gametangiophores fused together and new gametangiophores were often initiated from the old ones. Furthermore, Mpacl5 showed altered responses to heat and salt stresses. Given the absence of spermine in bryophytes, these results suggest that thermospermine has a dual primordial function in organ development and stress responses in M. polymorpha. The stress response function may have eventually been assigned to spermine during land plant evolution."
Author: Arpita Yadav
The Plant Cell (2023)
Excerpts: "Although the function of GAs in mediating light responses has been thoroughly investigated in angiosperms, its conservation across land plants is unclear. The presence of this pathway in extant bryophytes, such as the liverwort Marchantia polymorpha, would support the hypothesis that the function of GA in mediating light response has been conserved since the most recent common ancestor of the vascular and nonvascular plants that lived on lands more than 400 million years ago. In this issue, Rui Sun and colleagues (Sun et al. 2023) investigated the impact of gibberellin-related compounds on the response of M. polymorpha to FR light."
"Under conditions enriched with FR light, wild-type M. polymorpha plants displayed a growth pattern characterized by narrow and hyponastic thallus, along with the initiation of gametangiophore (sexual structures) formation. This was accompanied by an upregulation in the expression of genes involved in gibberellin biosynthesis and an accumulation of the GA precursor GA12. On the other hand, mutations in genes related to gibberellin biosynthesis, such as MpCPS, exhibited a wide and flat thallus and a delay in the formation of gametangiophores (Fig. 1). Introducing the GA precursor KA to the Mpcps mutants restored the wild-type phenotype in a dose-dependent manner. Interestingly, no active GAs from angiosperms could rescue the phenotype, suggesting that the mutant phenotypes were caused by a deficiency of KA-derived bioactive diterpenoid compound(s) referred to as GAMp."
"In the comparative analysis of GA-related diterpenoid biosynthesis in M. polymorpha and Physcomitrella patens, the authors observed conservation of components in the biosynthesis of KA. However, notable distinctions were identified in the synthesis of bioactive compounds derived from KA. GAs in vascular plants are detected through GID1 receptors. However, bryophytes do not possess these receptors, indicating distinct mechanisms for perceiving GAs and regulating responses to FR light. The hyponastic responses observed in M. polymorpha under FR light conditions, similar to A. thaliana and other land plants, are regulated by a single phytochrome (Mpphy) and a transcription factor, PHYTOCHROME-INTERACTING FACTOR (MpPIF), which is present in a single copy (Inoue et al. 2016, 2019). In this research, the authors found that the FR light-mediated biosynthesis of GAMp is also dependent on MpPIF."
Authors: Adrian S. Monthony, Maxime de Ronne and Davoud Torkamaneh.
bioRxiv (2023)
Abstract: "Sexual plasticity describes an organism's ability to change its phenotypic sex in response to environmental, chemical or physiological cues without a change in sex chromosome karyotype. Cannabis sativa L. (cannabis) is a medically important dioecious crop, with a pair of heteromorphic XY sex chromosomes. Cannabis has demonstrated sexual plasticity in response to chemical treatments which target the biosynthesis and signalling of ethylene. To date, ethylene biosynthesis and signalling has not been specifically studied in C. sativa, and the role of ethylene-related genes (ERGs) in sexual plasticity in the species has not been investigated. In the present study, we performed gene orthology analysis based on the model species Arabidopsis thaliana L. to reconstruct the C. sativa Yang Cycle, ethylene biosynthesis and ethylene signalling pathways, whose canonical composition appear conserved in cannabis. Additionally, we employ two transcriptomic datasets containing male, female and chemically induced male flowers to investigate patterns of expression for ethylene-related genes which may be involved in sexual plasticity. Comparison of these transcriptomes highlighted CsERGs whose differential expression was associated with sexual determination and those which we propose are associated with the sexual plasticity. These sexual plasticity ERGs could be classified into two patterns of expression: karyotype concordant (KC) and unique (uERG). We show that CsERGs involved in sexual plasticity are distributed throughout the genome and are not exclusive to the sex chromosomes, suggesting a broad control of sexual plasticity in C. sativa."
Author: Pamela J. Hines.
Science (2022)
Text: "In melons, flowers initially develop bisexually, but further growth brings arrest of either carpel or stamen development, refining mature flowers into male or female. Only the female flowers produce melons. Zhang et al. have identified the genes involved in turning the bisexual primordial flower into either a male or female flower. The zinc finger transcription factor WIP1 interferes with carpel development, allowing male flower development to proceed. Conversely, expression of an enzyme involved in producing the hormone ethylene, perhaps supported by auxin signaling, supports and promotes female flower development."
Authors: Cecilia Martínez, Alicia García and Manuel Jamilena.
In Book: "Ethylene in Plant Biology" (2022). Editors: Samiksha Singh, Tajammul Husain, Vijay Pratap Singh, Durgesh Kumar Tripathi, Sheo Mohan Prasad and Nawal Kishore Dubey.
Abstract: "Ethylene is a plant phytohormone that regulates multiple aspects of plant growth and development. In this chapter, we review the involvement of this essential hormone in different valuable agronomic traits during reproductive development. Ethylene controls the transition between vegetative and reproductive stages of development in some plant species and has an essential role in the female flowering transition of monoecious cucurbits. During flower development, ethylene modulates the growth and maturation of sexual organs and petals up to anthesis. Transcriptomic analyses, ethylene mutants, and the external application of ethylene promoters and inhibitors have demonstrated that ethylene regulates stamen filament elongation, anther and pollen development and maturation, pistil and ovule formation and maturation, and the expansion, senescence, and abscission of petals. Recently it has been demonstrated that the successful pollination and fertilization events that trigger fruit set and early fruit development in species like tomato and zucchini are also dependent on reduced production of ethylene in flowers and that in the absence of pollination and parthenocarpy, a burst of ethylene is induced that participates in the abortion and senescence of the ovary. One of the most remarkable roles of ethylene in flower and fruit development has been thoroughly studied in the monoecious species of the Cucurbitaceae family, where ethylene biosynthesis and perception genes have been discovered that are responsible for sex determination. The chapter also underlines the importance of these discoveries in improving the reproduction and performance of different crop species."
Authors: Gustavo Cebrián, Jessica Iglesias-Moya, Jonathan Romero, Cecilia Martínez, Dolores Garrido and Manuel Jamilena.
Frontiers in Plant Science (2022)
Abstract: "A methanesulfonate-generated mutant has been identified in Cucurbita pepo that alters sex determination. The mutation converts female into hermaphrodite flowers and disrupts the growth rate and maturation of petals and carpels, delaying female flower opening, and promoting the growth rate of ovaries and the parthenocarpic development of the fruit. Whole-genome resequencing allowed identification of the causal mutation of the phenotypes as a missense mutation in the coding region of CpACO1A, which encodes for a type I ACO enzyme that shares a high identity with Cucumis sativus CsACO3 and Cucumis melo CmACO1. The so-called aco1a reduced ACO1 activity and ethylene production in the different organs where the gene is expressed, and reduced ethylene sensitivity in flowers. Other sex-determining genes, such as CpACO2B, CpACS11A, and CpACS27A, were differentially expressed in the mutant, indicating that ethylene provided by CpACO1A but also the transcriptional regulation of CpACO1A, CpACO2B, CpACS11A, and CpACS27A are responsible for determining the fate of the floral meristem toward a female flower, promoting the development of carpels and arresting the development of stamens. The positive regulation of ethylene on petal maturation and flower opening can be mediated by inducing the biosynthesis of JA, while its negative control on ovary growth and fruit set could be mediated by its repressive effect on IAA biosynthesis."
Authors: Jian Pan, Haifan Wen, Guanqun Chen, Wenhui Lin, Hui Du, Yue Chen, Leyu Zhang, Hongli Lian, Gang Wang, Run Cai and Junsong Pan.
Plant Physiology (2021)
Abstract: "Sex determination is a crucially important developmental event that is pervasive throughout nature and enhances the adaptation of species. Among plants, cucumber (Cucumis sativus L.) can generate both unisexual and bisexual flowers, and the sex type is mainly controlled by several 1-aminocyclopropane-1-carboxylic acid (ACC) synthases. However, the regulatory mechanism of these synthases remains elusive. Here, we used gene expression analysis, protein-DNA interaction assays and transgenic plants to study the function of a gynoecium-specific gene, ETHYLENE RESPONSE FACTOR31 (CsERF31), in female flower differentiation. We found that in a predetermined female flower, ethylene signalling activates CsERF31 by CsEIN3, and then CsERF31 stimulates CsACS2, which triggers a positive feedback loop to ensure female rather than bisexual flower development. A similar interplay is functionally conserved in melon (Cucumis melo L.). Knockdown of CsERF31 by RNAi causes defective bisexual flowers to replace female flowers. Ectopic expression of CsERF31 suppresses stamen development and promotes pistil development in male flowers, demonstrating that CsERF31 functions as a sex switch. Taken together, our data confirm that CsERF31 represents the molecular link between female-male determination and female-bisexual determination, and provide mechanistic insight into how ethylene promotes female flowers, rather than bisexual flowers, in cucumber sex determination."
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