Abstract
Key message
The developmental morphology of male and female kiwifruit flowers is tracked to delimit a framework of events to aid the study of divergence in floral gene expression.
Abstract
The transition from hermaphrodite to unisexual development of kiwifruit (Actinidia chinensis Planch) flowers has been reported previously, but differences in gene expression controlling sexual development for this species have not been associated with the major developmental changes occurring within pistils. We investigated the key stages in male and female flower development to define the point at which meristematic activities diverge in the two sexes. A combination of scanning electron microscopy and light microscopy was used to investigate pistil development from the earliest stages. We identified seven distinct stages characterized by differences in ovary size and shape, macrosporogenesis, ovule primordium development, anther locule lengthening, microspore wall thickening, and pollen degeneration. Sex differences were evident from the initial stage of development, with a laterally compacted gynoecium in male flowers. However, the key developmental stage, at which tissue differentiation clearly deviated between the two sexes, was stage 3, when flowers were 3.5 to 4.5 mm in length at approximately 10 d from initiation of stamen development. At this stage, male flowers lacked evident carpel meristem development as denoted by a lack of ovule primordium formation. Pollen degeneration in female flowers, probably driven by programmed cell death, occurred at the late stage 6, while the final stage 7 was represented by pollen release. As the seven developmental stages are associated with specific morphological differences, including flower size, the scheme suggested here can provide the required framework for the future study of gene expression during the regulation of flower development in this crop species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ainsworth CC, Crossley S, Buchanan-Wollaston V, Thangavelu M, Parker J (1995) Male and female flower in the dioecious plant sorrel show different pattern of MADS box genes expression. Plant Cell 7:1583–1598
Akagi T, Henry IM, Ohtani H, Morimoto T, Beppu K, Kataoka I, Tao R (2018) A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit. Plant Cell 30:780–795
Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126(11):2377–2386
Biasi R, Falasca G, Speranza A, De Stradis A, Scoccianti V, Franceschetti M, Bagni N, Altamura MM (2001) Biochemical and ultrastructural features related to male sterility in the dioecious species Actinidia deliciosa. Plant Physiol Biochem 39(1):395–406
Brundel DJ (1975) Flower development of the Chinese Gooseberry (Actinidia chinensis Planch). N Z J Bot 13:485–496
Canas LA, Busscher M, Angenent GC, Beltran JP, Van Tunen AJ (1993) Nuclear localization of petunia MADS box protein FBP1. Plant J 6:597–604
Caporali E, Carboni A, Galli MG, Rossi G, Spada A, Lomgo MGP (1994) Development of male and female flowers in Asparagus officinalis. Search of transition from hermaphroditic to unisexual development pathway. Sex Plant Reprod 7:239–249
Caporali E, Spada A, Marziani G (2002) Unisexual flower development: different strategies for the elimination of useless organs. Flower Newsl 33:33–41
Caporali E, Spada A, Marziani G, Failla O, Scienza A (2003) The arrest of development of abortive reproductive organs in the unisexual flore of Vitis vinifera spp. silvestris. Sex Plant Reprod 15:291–300
Coimbra S, Torrao L, Abreu I (2004) Programmed cell death induces male sterility in Actinidia deliciosa female flowers. Plant Physiol Biochem 42:537–541
Crowhurst RN, Gleave AP, MacRae EA, Ampomah-Dwamena C, Atkinson RG, Beuning LL, Bulley SM, Chagne D, Marsh KB, Matich AJ, Mantefiori M, Newcomb RD, Schaffer RJ, Usadel B, Allan AC, Bolding HL, Bowen JH, Davy MW, Eckoff R, Ferguson AR, Fraser LG, Gera E, Hellens RR, Janssen BB, Klages K, Lo RK, MacDiarmid RM, Nain B, Mcneilage MA, Rasdsan M, Richardson AC, Rikkerink EHA, Ross GS, Schroder R, Snowden KC, Souleyre EJF, Templeton MD, Walton EF, Wang D, Wang MY, Wang YY, Wood M, Wu R, Yauk Y, Laing WA (2008) Analysis of expressed sequence tag from Actinidia: application of a cross species EST database for gene discovery in the areas of flavor, health, color and ripening. BMC Genom 9:351
Falasca G, D’Angeli S, Biasi R, Fattorini L, Matteucci M, Canini A, Altamura MM (2013) Tapetum and middle layer control male fertility in Actinidia deliciosa. Ann Bot 112:1046–1055
Ferguson AR (1984) Kiwifruit: a botanical review. Hortic Rev 6:1–64
Fraser LG, Tsang GK, Datson PM, De Silvia HN, Havery CF, Geoffrey GP, Crowhurst RN, McNeilage MM (2009) A gene linkage map in the dioecious species Actinidia chinensis reveal putative X/Y sex-determinant chromosomes. BMC Genom 10:102
Grant S, Hunkirchen B, Saedler H (1994) Developmental difference between male and female flowers in the dioecious plant Silene latifolia. Plant J 6:471–480
Hardenak S, Ye D, Saedler H, Grant S (1994) Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant white campion. Plant Cell 6:1775–1777
Harvey CF, Fraser LG (1988) Floral biology of two species of Actinidia (Actinidiaceae) II early embryogenesis. Bot Gaz 149:37–44
Huang HW, Ferguson AR (2007) Genetic resources of kiwifruit: domestication and breeding. Hortic Rev 33:1–121
Huang SX, Ding J, Deng DJ, Tang W, Sun HH, Liu DY et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun. 4:2640
Kamiuchi Y, Yaqmamoto K, Furutani M, Tasaka M, Aida M (2014) The CUC 1 and CUC2 genes promote carpel margin meristem formation during Arabidopsis gynoecium development. Front Plant Sci 5:165
Kim SC, Uhm YK, Ko S, Oh CJ, Kwack Y, Kim HL, Lee Y, An CS, Park PB, Kim HB (2015) KiwiPME1 encoding pectin methylesterase is specifically expressed in the pollen of a dioecious plant species, kiwifruit (Actinidia chinensis). Hortic Environ Biotechnol 56:402–410
Maheshwari P (1950) An introduction to the embryology of angiosperms. McGraw-Hill, New York
Matsunaga S, Kawano S (2001) Sex determination by sex chromosome in dioecious plants. Plant Biol. 3(5):481–488
Messina R (1993) Microsporogenesis in male-fertile cv. Matua and male-sterile cv. Hayward of Actinidia deliciosa var. deliciosa (Kiwifruit). Adv Hortic Sci 7(2):77–81
Pilkington S, Crowhurst R, Hilario E et al (2018) A manually annotated Actinidia chinensis var. chinensis (kiwifruit) genome highlights the challenges associated with draft genomes and gene prediction in plants. BMC Genom 19(1):257. https://doi.org/10.1186/s12864-018-4656-3
Ramos MJN, Coito JL, Gomes Silva H, Cunha J, Ribero Costa MM, Rocheta M (2014) Flower development and sex specification in wild grapevine. BMC Genom 15:1095–1116. https://doi.org/10.1186/1471-2164-15-1095
Reyes-Olalde JI, Zuñiga-Mayo VM, Serwatowska J, Chavez Montes AR, Lozano Sotomayor P, Herrera-Ubaldo H, Gonzalez-Aguilera LK, Ballester P, Ripoll JJ, Ezquer I, Paolo D, Heyl A, Colombo L, Colombo L, Yanofsky MF, Ferrandiz C, Marsch-Martinez N, De Folter S (2017) The bHLH transcription factor SPATULA enables cytokinin signaling, and both activate auxin biosynthesis and transport genes at the medial domain of the gynoecium. PLoS Genet. https://doi.org/10.1371/journal.pgen.1006726
Scaglione D, Fornasiero A, Spadotto A, Cattonaro F, Pinto C, Infante R, Meneses C, Messina R, Lain O, Cipriani G, Testolin R (2015) A RAD-based linkage map of kiwifruit (Actinidia chinensis Pl.) as a tool to improve the genome assembly and to scan the genomic region of the gender-determinant for the marker-assisted breeding. Tree Genet Genomes 11:115. https://doi.org/10.1007/s11295-015-0941-3
Shera B, Franks RG (2015) Auxin and cytokinin act during gynoecioum patytering and development of ovuke from the meristematic medial domain. Wiley Interdiscip Rev Dev Biol. 4(6):555–571. https://doi.org/10.1002/wdev.193
Sobral R, Silva HG, Cecílio LM, Costa MMR (2016) The quest for molecular regulation underlying unisexual flower development. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00160
Tang P, Zhang Q (2017) Comparative transcript profiling explores differentially expressed genes associated with sexual phenotype in Kiwi. PLoS ONE 12(7):e0180542
Testolin R, Cipriani G (2016) Markers, maps, and marker-assisted selection: 259–264. In: Testolin R, Huang HW, Ferguson AR (eds) The kiwifruit genome. Series compendium of plant genomes. Springer, Basel. https://doi.org/10.1007/978-3-319-32274-2. ISBN 978-3-319-32272-8
Varkonyi-Gasic E, Moss E, Voogd C, Wu R, Hlough R, Wang Y, Hellens R (2011) Identification and characterization of flowering genes in kiwifruit: sequence conservation and role in kiwifruit flower development. BMC Plant Biol 11:72. https://doi.org/10.1186/1471-2229-11-72
Wang T, Gleave AP (2012) Application of biotechnology in kiwifruit (Actinidia). In: Agbo EC (ed) Innovations in Biotechnology, In Tech. ISBN 978-953-51-0096-6
White J (1990) Pollen development in Actinidia deliciosa var. deliciosa: histochemistry of the Microspore Mother Cell Walls. Ann Bot 65(3):231–239
Zhang Q, Liu CY, Liu YF, VanBuren R, Yao XH, Zhong CH et al (2015) High-density interspecific genetic maps of kiwifruit and the identification of sex-specific markers. DNA Res 22:367–375. https://doi.org/10.1093/dnares/dsv019
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Lars Ostergaard.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Caporali, E., Testolin, R., Pierce, S. et al. Sex change in kiwifruit (Actinidia chinensis Planch.): a developmental framework for the bisexual to unisexual floral transition. Plant Reprod 32, 323–330 (2019). https://doi.org/10.1007/s00497-019-00373-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-019-00373-w