Abstract
A proper development of the male and female germlines is key to the reproductive success of plants. As a result of the development of the male and female germlines the male (pollen) and female (embryo sac) gametophytes will be produced. After pollination, pollen–pistil interaction, fertilization, embryogenesis, and finally, the formation of the persistent propagule – the seed will take place. During reproductive cell development in angiosperms, male and female germlines develop inside the sporophytic tissues. The male germline develops in the anther surrounded by the tapetum whereas the female germline initiates in the nucellus composed of a single or several layers of somatic cells of the ovule. Initially, the cells that will remain somatic and those that will develop in the germlines are morphologically identical. But, later on, cell differentiation starts with the transition from somatic to reproductive fate and remarkable differences arise during germline development and mainly after meiosis. Such differences are also observed in the somatic cells that surround the germline and are closely linked to the crosstalk between the sporophyte tissues and the germline, a key process for the formation of the male and female gametes.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Albert B, Ressayre A, Nadot S (2011) Correlation between pollen aperture pattern and callose deposition in late tetrad stage in three species producing atypical pollen grains. Am J Bot 98:189–196
Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349
Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328
Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toryyama K (2005) The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation. Sex Plant Reprod 18:1–7
Armenta-Medina A, Demesa-Arévalo E, Vielle-Calzada JP (2011) Epigenetic control of cell specification during female gametogenesis. Sex Plant Reprod 24:137–147
Bachelier JB, Friedman WE (2011) Female gamete competition in an ancient angiosperm lineage. Proc Natl Acad Sci 108:12360–12365
Bajon C, Horlow C, Motamayor JC, Sauvanet A, Robert D (1999) Megasporogenesis in Arabidopsis thaliana L.: an ultrastructural study. Sex. Plant Reprod 12:99–109
Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, Gasser CS (1997) Interactions among genes regulating ovule development in Arabidopsis thaliana. Genetics 145:1109–1124
Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80
Bencivenga S, Simonini S, Benková E, Colombo L (2012) The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell 24:2886–2897
Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174:483–498
Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727
Cao L, Wang S, Venglat P, Zhao L, Cheng Y, Ye S, Ye S, Qin Y, Datla R, Zhou Y (2018) Arabidopsis ICK/KRP cyclin-dependent kinase inhibitors function to ensure the formation of one megaspore mother cell and one functional megaspore per ovule. PLoS Genet 14:e1007230
Carman JG, Crane CF, Riera-Lizarazu O (1991) Comparative histology of cell walls during meiotic and apomeiotic megasporogenesis in two hexaploid Australasian Elymus species. Crop Sci 31:1527
Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774
Cecchetti V, Celebrin D, Napoli N, Ghelli R, Brunetti P, Costantino P, Cardarelli M (2017) An auxin maximum in the middle layer controls stamen development and pollen maturation in Arabidopsis. New Phytol 213:1194–1207
Clement C, Audran JC (1995) Anther wall layers control pollen sugar nutrition in Lilium. Protoplasma 187:172–181
Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58:4027–4035
Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis somatic embryogenesis receptor kinases1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361
Costa ML, Sobral R, Ribeiro Costa MM, Amorim MI, Coimbra S (2015) Evaluation of the presence of arabinogalactan proteins and pectins during Quercus suber male gametogenesis. Ann Bot 115:81–92
Echlin P (1971) The role of the tapetum during microsporogenesis of angiosperms. In: Pollen. Butterworth-Heinemann, Oxford, pp 41–61
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168
Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58:333–349
Feng XL, Ni WM, Elge S, Mueller-Roeber B, Xu ZH, Xue HW (2006) Auxin flow in anther filaments is critical for pollen grain development through regulating pollen mitosis. Plant Mol Biol 61:215–226
Forestan C, Farinati S, Varotto S (2012) The maize PIN gene family of auxin transporters. Front Plant Sci 3:16
Franchi G, Pacini E (1993) Role of the tapetum in pollen and spore dispersal. Plant Syst Evol 7:1–11
Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013
Friis EM, Crane PR, Pedersen KR (2019) The endothelium in seeds of early angiosperms. New Phytol 224:1419–1424
Gaiser JC, Robinson-Beers K, Gasser CS (1995) The Arabidopsis SUPERMAN gene mediates asymmetric growth of the outer integument of ovules. Plant Cell 7:333–345
Gasser CS, Broadhvest J, Hauser BA (1998) Genetic analysis of ovule development. Annu Rev Plant Physiol Plant Mol Biol 49:1–24
Gómez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57:876–891
Gross-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes Dev 16:1129–1138
Harder L, Johnson S (2008) Function and evolution of aggregated pollen in angiosperms. Int J Plant Sci 169:59–78
Heslop-Harrison J (1979) The forgotten generation: some thoughts on the genetics and physiology of angiosperm gametophytes. In: The Bateson lecture: proceedings of the fourth John Innes symposium, pp 1–14
Hofmesiter W (1851) Vergleichende Untersuchungen der Keimung, Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farrn, Equisetaceen, Rhizokarpeen and Lykopodiaceen) und der Samenbildung der Coniferen. Friedrich Hofmeister, Leipzig
Hong L, Tang D, Shen Y, Hu Q, Wang K, Li M, Lu T, Chang Z (2012) MIL2 (MICROSPORELESS2) regulates early cell differentiation in the rice anther. New Phytol 196:402–413
Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci U S A 105:2220–2225
Juranic M, Tucker MR, Schultz CJ, Shirley NJ, Taylor JM, Spriggs A, Johnson SD, Bulone V, Koltunow AM (2018) Asexual female gametogenesis involves contact with a sexually-fated megaspore in apomictic Hieracium. Plant Physiol 177:1027–1049.
Kapil RN, Tiwari SC (1978) The integumentary tapetum. Bot Rev 44:457–490
Kelley DR, Gasser CS (2009) Ovule development: genetic trends and evolutionary considerations. Sex Plant Reprod 22:229–234
Kinoshita-Tsujimura K, Kakimoto T (2011) Cytokinin receptors in sporophytes are essential for male and female functions in Arabidopsis thaliana. Plant Signal Behav 6:66–71
Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96
Lehman TA, Sanguinet KA (2019) Auxin and cell wall crosstalk as revealed by the Arabidopsis thaliana cellulose synthase mutant radially swollen 1. Plant Cell Physiol 60:1487–1503
Leszczuk A, Szczuka E (2018) Arabinogalactan proteins: immunolocalization in the developing ovary of a facultative apomict Fragaria x ananassa (Duch.). Plant Physiol Biochem 123:24–33
Lieber D, Lora J, Schrempp S, Lenhard M, Laux T (2011) Arabidopsis WIH1 and WIH2 genes act in the transition from somatic to reproductive cell fate. Curr Biol 21:1009–1017
Lituiev DS, Krohn NG, Müller B, Jackson D, Hellriegel B, Dresselhaus T, Grossniklaus U (2013) Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte. Development 140:4544–4553
Lora J, Hormaza JI (2018) Pollen wall development in mango (Mangifera indica L., Anacardiaceae). Plant Reprod 31(4):385–397, 1–13
Lora J, Testillano PS, Risueño MC, Hormaza JI, Herrero M (2009) Pollen development in Annona cherimola Mill. (Annonaceae). Implications for the evolution of aggregated pollen. BMC Plant Biol 9:129
Lora J, Hormaza JI, Herrero M, Gasser CS (2011) Seedless fruits and the disruption of a conserved genetic pathway in angiosperm ovule development. Proc Natl Acad Sci U S A 108:5461–5465
Lora J, Herrero M, Hormaza JI (2014) Microspore development in Annona (Annonaceae): differences between monad and tetrad pollen. Am J Bot 101:1508–1518
Lora J, Hormaza JI, Herrero M (2016) The diversity of the pollen tube pathway in plants: toward an increasing control by the sporophyte. Front Plant Sci 7:107
Lora J, Herrero M, Tucker MR, Hormaza JI (2017) The transition from somatic to germline identity shows conserved and specialized features during angiosperm evolution. New Phytol 216:495–509
Lora J, Laux T, Hormaza JI (2019a) The role of the integuments in pollen tube guidance in flowering plants. New Phytol 221:1074–1089. https://doi.org/10.1111/nph.15420
Lora J, Yang X, Tucker MR (2019b) Establishing a framework for female germline initiation in the plant ovule. J Exp Bot 70:2937–2949
Ma J, Duncan D, Morrow DJ, Fernandes J, Walbot V (2007) Transcriptome profiling of maize anthers using genetic ablation to analyze pre-meiotic and tapetal cell types. Plant J 50:637–648
Maciel-Silva AS, Porto KC (2014) Reproduction in bryophytes. In: Ramawat KG, Mérillon JM, Shivanna KR (eds) Reproductive biology of plants. Taylor & Francis, New York
Maheshwari P (1950) An introduction to the embryology of angiosperms. McGraw-Hill, New York
Marsch-Martínez N, Ramos-Cruz D, Irepan Reyes-Olalde J, Lozano-Sotomayor P, Zúñiga-Mayo VM, de Folter S (2012) The role of cytokinin during Arabidopsis gynoecia and fruit morphogenesis and patterning. Plant J 72:222–234
McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275
Medina FJ, Risueño MC, Rodriguez-Garsia MI (1981) Evolution of the cytoplasmic organelles during female meiosis in Pisum sativum L. Planta 151:215–225
Nepi M, Franchi GG, Pacini E (2001) Pollen hydration status at dispersal: cytophysiological features and strategies. Protoplasma 216:171–180
Nonomura KI, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739
Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684
Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632
Pacini E (1990) Tapetum and microspore function. In: Microspores: evolution and ontogeny. Academic Press, London, pp 213–237
Pacini E, Franchi GG (1988) Amylogenesis and amylolysis during pollen grain development. In: Sexual reproduction in higher plants. Springer, Berlin, pp 181–186
Pacini E, Franchi GG, Hesse M (1985) The tapetum - its form, function, and possible phylogeny in embryophyta. Plant Syst Evol 149:155–185
Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228:73–77
Peel MD, Carman JG, Leblanc O (1997) Megasporocyte callose in apomictic buffelgrass, Kentucky bluegrass, Pennisetum squamulatum Fresen, Tripsacum L., and weeping lovegrass. Crop Sci 37:724
Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446
Pinto SC, Mendes MA, Coimbra S, Tucker MR (2019) Revisiting the female germline and its expanding toolbox. Trends Plant Sci 24:455–467
Polowick PL, Sawhney VK (1993) Differentiation of the tapetum during microsporogenesis in tomato (Lycopersicon esculentum Mill.), with special reference to the tapetal cell wall. Ann Bot 72:595–605
Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460
Quilichini TD, Douglas CJ, Samuels AL (2014) New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann Bot 114:1189–1201
Raghavan V (1988) Anther and pollen development in rice (Oryza sativa). Am J Bot 75:183–196
Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133:1170–1180
Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54
Rodkiewicz B (1970) Callose in cell walls during megasporogenesis in angiosperms. Planta 93:39–47
Rudall PJ (1997) The nucellus and chalaza in monocotyledons: structure and systematics. Bot Rev 63:140–181
Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63
Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 96:11664–11669
Schmidt A, Wuest S, Vijverberg K, Baroux C, Grossniklaus U (2011) Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol 9:e1001155
Schneitz K, Hulskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7:731–749
Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN (1996) The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics 142:1009–1020
Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–941
Shi J, Cui M, Yang L, Kim YJ, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci 20:741–753
Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423
Sporne KR (1969) The ovule as an indicator of evolutionary status in angiosperms. New Phytol 68:555–566
Takaso T, Bouman F (1986) Ovule and seed ontogeny in Gnetum gnemon L. Bot Mag (Tokyo) 99:241–266
Tucker MR, Koltunow AM (2014) Traffic monitors at the cell periphery: the role of cell walls during early female reproductive cell differentiation in plants. Curr Opin Plant Biol 17:137–145
Tucker MR, Paech NA, Willemse MT, Koltunow AM (2001) Dynamics of callose deposition and beta-1,3-glucanase expression during reproductive events in sexual and apomictic Hieracium. Planta 212:487–498
Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AM (2012a) Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–1404
Tucker MR, Okada T, Johnson SD, Takaiwa F, Koltunow AM (2012b) Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium. J Exp Bot 63:3229–3241
Walker JW, Doyle JA (1975) The bases of angiosperm phylogeny: palynology. Ann Missouri Bot Gard 62:664
Wang CJ, Nan GL, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–2603
Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39
Xu J, Yang C, Yuan Z, Zhang D, Gondwe MY, Ding Z, Liang W, Zhang D, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22:91–107
Xu J, Ding Z, Vizcay-Barrena G, Shi J, Liang W, Yuan Z, Werck-Reichhart D, Schreiber L, Wilson ZA, Zhang D (2014) ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26:1544–1556
Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117
Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804
Yang SL, Jiang L, Puah CS, Xie LF, Zhang XQ, Chen LQ, Yang WC, Ye D (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells. Plant Physiol 139:186–191
Yao X, Yang H, Zhu Y, Xue J, Wang T, Song T, Yang Z, Wang S (2018) The canonical E2Fs are required for germline development in Arabidopsis. Front Plant Sci 9:638
Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095
Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yanf ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52:528–538
Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031
Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Hervé P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–387
Zhao X, Bramsiepe J, Van Durme M, Komaki S, Prusicki MA, Maruyama D, Forner J, Medzihradszky A, Wijnker E, Harashima H, Lu Y, Schmidt A, Guthörl D, Sahún-Logroño R, Guan Y, Pochon G, Grossniklaus U, Laux T, Higashiyama T, Lohmann JU, Nowack MK, Schnittger A (2017) Retinoblastoma related1 mediates germline entry in Arabidopsis. Science 356:eaaf6532
Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in Tapetal Development and Function 1 is essential for another development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277
Zhu J, Lou Y, Xu X, Yang ZN (2011) A genetic pathway for tapetum development and function in Arabidopsis. J Integr Plant Biol 53:892–900
Zurcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Muller B (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161:1066–1075
Acknowledgements
This work was supported by Ministerio de Economía y Competitividad – European Regional Development Fund, European Union (AGL2015-74071-JIN, AGL2016-77267-R, PDI2019-109566RB-IOO) and Junta de AndalucÚa (P18-RT-3272).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Lora, J., Hormaza, J.I. (2020). Crosstalk Between the Sporophyte and the Gametophyte During Anther and Ovule Development in Angiosperms. In: Cánovas, F.M., Lüttge, U., Risueño, MC., Pretzsch, H. (eds) Progress in Botany Vol. 82. Progress in Botany, vol 82. Springer, Cham. https://doi.org/10.1007/124_2020_50
Download citation
DOI: https://doi.org/10.1007/124_2020_50
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-68619-2
Online ISBN: 978-3-030-68620-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)