Female gametogenesis and early seed development in Amaranthus hypochondriacus L.

Angelica Barrales-López, Lorenzo Guevara-Olvera, Eduardo Espitia-Rangel, Mario M. González-Chavira, Aurea Bernardino-Nicanor, Leopoldo Gonzalez-Cruz, Wilson Huanca-Mamani, Gerardo Acosta-García

Abstract


Background: Attention to amaranth grains has increased in recent years due to the nutritional value of their seed proteins, which have high levels of the amino acid lysine. However, there is no detailed study describing the stages of seed development in Amaranthus hypochondriacus.

Question: How are the developmental patterns of the female gametophyte and young seed in Amaranthus hypochondriacus?

Species studied: Amaranthus hypochondriacus L ’Revancha’ (Amaranthaceae).

Study site and years of study: Plants were growth and collected from 2014 to 2016, in a greenhouse at Instituto Tecnológico de Celaya, Guanajuato, Mexico.

Methods: Glomerules were collected before pollination and two weeks after anthesis. The ovules at different development stages were fixed and cleared and were analyzed by light microscopy. A clearing protocol was used to observe the developmental stages during female gametogenesis and embryogenesis.

Results: We observed that the Amaranthus hypochondriacus ovule has a campylotropous form. The female gametophyte showed a Polygonum-type pattern of development. We were also able to identify all the stages from the megaspore mother cell to the cotyledon embryo stage. After meiosis, the micropylar megaspore differentiates into the functional megaspore. The embryo did not show symmetric divisions, although the final pattern is similar to that of in eudicotyledons. The suspensor showed additional longitudinal divisions, giving rise to a 2-rowed suspensor, while the endosperm showed a helobial development.

Conclusions: These results will be used as baseline to identify morphological changes during seed development and to develop new strategies to improve seed quality or increase the yield.


Keywords


Amaranth; embryogenesis; megagametogenesis; megasporogenesis

Full Text:

PDF Supplementary_data

References


Bartoli G, Felici C, Castiglione RM. 2017. Female gametophyte and embryo development in Helleborus bocconei Ten. (Ranunculaceae). Protoplasma 254: 491-504. DOI: 10.1007/s00709-016-0969-8

Burrieza HP, López-Fernández MP, Maldonado S. 2014. Analogous reserve distribution and tissue characteristics in quinoa and grass seeds suggest convergent evolution. Frontiers in Plant Science 5: 1-11. DOI:10.3389/fpls.2014.00546

Bouman F. 1984. The ovule. In: Johri BM, ed. Embryology of angiosperms. Berlin: Springer. DOI: 10.1007/978-3-642-69302-1; ISBN: 978-3-642-69304-5

Chehregani A, Malayeri B, Yousef N. 2009. Developmental Stages of Ovule and Megagametophyte in Chenopodiumbotrys L. (Chenopodiaceae). Turkish Journal of Botany 33: 75-81. DOI: 10.3906/bot-0805-20

Coimbra S, Salema R. 1994. Amaranthus hypochondriacus: seed structure and localization of seed reserves. Annals of Botany 74: 373-379. DOI: 10.1006/anbo.1994.1130

Coimbra S, Salema R. 1997. Immunolocalization of arabinogalactan proteins in Amaranthus hypochondriacus L ovules. Protoplasma 199: 75-82. DOI:10.1007/BF02539808

Coimbra S, Salema R. 1999. Ultrastructure of the developing and fertilized embryo sac of Amaranthus hypochondriacus L. Annals of Botany 84: 781-789. DOI: 10.1006/anbo.1999.0978

Das S. 2016. Amaranths: the crop of great prospect. In: Das S, ed. Amaranthus: a promising crop of future. Singapore: Springer. 13-48. DOI: 10.1007/978-981-10-1469-7; ISBN: 978-981-10-1468-0

García-Campayo V, Demesa-Arévalo E, Huanca-Mamani W, Vielle-Calzada JP. 2011. Female gametogenesis and early seed formation in plants. In: Chimal-Monroy J, ed. Topics in animal and plant development: from cell differentiation to morphogenesis. Kerala India: Transworld Research Network. 93-111. ISBN: 978-81-7895-506-3

Guo A, Zheng CX. 2013. Female gametophyte development. Journal of Plant Biology 56: 345-356. DOI: 10.1007/s12374-013-0131-5

Espitia-Rangel E. 2016. Etnología del amaranto. Arqueología 138: 64-70.

Huerta OJA, Barba de la Rosa AP. 2012. Caracterización bioquímica y estructural de las proteínas de reserva de amaranto. In: Espitia-Rangel E, ed. Amaranto; Ciencia y Tecnología. México: INIFAP/SINAREFI. 293-302. DOI: 10.13140/2.1.2981.9684

Huerta OJA, Maldonado CE, Barba de la Rosa AP. 2012. Amaranto: propiedades benéficas para la salud. In: Espitia-Rangel E, ed. Amaranto; Ciencia y Tecnología. México: INIFAP/SINAREFI. 303-312. DOI: 10.13140/2.1.2981.9684

Janssen F, Pauly A, Rombouts I, Jansens KJA, Deleu LJ, Delcour JA. 2017. Proteins of Amaranth (Amaranthus spp.), Buckwheat (Fagopyrumspp.), and Quinoa (Chenopodiumspp.): A Food Science and Technology Perspective. Comprehensive Review in Food Science and Food Safety 16: 39-58. DOI: 10.1111/1541-4337.12240

Johansen DA. 1940. Plant microtechnique. New York: McGraw-Hill Book Co.

Joshi AC. 1936. A note on the antipodals of Digeria arvensis Forsk. Current Science 4: 741-742.

Joshi AC, Kajale LB. 1937. Fertilization and seed development in Amaranthaceae. Proceedings of the Indian Academy of Sciences 5: 91–100.

Kajale LB. 1935. The female gametophyte of Alternanthera sessilis R Br. Proceedings of the Indian Academy of Sciences 2: 476-480.

Kajale LB. 1940. A contribution to the embryology of the Amaranthaceae. Proceedings of the Indian Academy of Sciences 6: 597-625.

Kajale LB. 1954. The antipodals in the family Amaranthaceae. Current Science 23: 165-166.

López-Fernández MP, Maldonado S. 2013a. Programmed cell death during quinoa perisperm development. Journal of Experimental Botany 57: 3747–3753. DOI: 10.1093/jxb/ert170

López-Fernández MP, Maldonado S. 2013b. Ricinosomes provide an early indicator of suspensor and endosperm cells destined to die during late seed development in quinoa (Chenopodium quinoa). Annals of Botany 112: 1253–1262. DOI:10.1093/aob/mct184

McClung de Tapia E, Matínez DY, Ibarra EM, Adriano CCM. 2014. Los orígenes prehispánicos de una tradición alimentaria en la Cuenca de México. Anales de Antropología 48: 97-121. DOI: 10.1016/S0185-1225(14)70491-6

Moco MCC, Marianth JEA. 2004. Female gametophyte development in Adesmialatifolia (Spreng) Vog (Leguminosae – Papilionoideae). Revista Brasileira de Botânica 27: 241-248. DOI: 10.1590/S0100-84042004000200004.

Morales-Guerrero JC, Vázquez-Mata N, Castignoli RB. 2009. El Amaranto, características físicas, químicas, toxicológicas y funcionales y aporte nutricio. México: Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán. ISBN: 9786077797005 6077797006

Olufolaji AO, Odeleye FO. 2011. Evaluation of the maturity of seeds from different sections of inflorescences of Amaranthus cruentus and Celosia argentea. Agriculture and Biology Journal of North America 4: 459-467. DOI: 10.5251/abjna. 2013.4.4.459.467.

Pal A, Singh RP, Pal M. 1990. Development and structure of seeds in Amaranthus hypochondriacus L. and its wild progenitor A. hybridus L. Phytomorphology 40: 145–150.

Prego I, Maldonado S, Otegui M. 1998. Seed structure and localization of reserves in Chenopodium quinoa. Annals of Botany 82: 481–488. DOI: 10.1006/anbo.1998.0704

Salinas-Gamboa R, Johnson SD, Sánchez-León N, Koltunow AMG, Vielle-Calzada JP. 2016. New observations on gametogenic development and reproductive experimental tools to support seed yield improvement in cowpea [Vigna unguiculata (L.) Walp.] Plant Reproduction 29: 165-177. DOI: 10.1007/s00497-015-0273-3

Silva-Sánchez C, Barba de la Rosa AP, León-Galván MF, De Lumen BO, De León-Rodríguez A, González de Mejía E. 2008. Bioactive peptides in amaranth (Amaranthus hypochondriacus) seed. Journal of Agricultural and Food Chemistry 56: 1233-1240. DOI: 10.1021/jf072911z

Talamali A, Gorenflot R, Haicour R, Henry Y, Dutuit P. 2007. Embryogenesis of Atriplexhalimus L. (Amaranthaceae). Acta Botanica Gallica 154: 651-659. DOI: 10.1080/12538078.2007.10516086

Zhao P, Begcy K, Dresselhaus T, Sun MX. 2017. Does Early Embryogenesis in Eudicots and Monocots Involve the Same Mechanism and Molecular Players. Plant Physiology 173: 130–142. DOI: 10.1104/pp.16.01406




DOI: http://dx.doi.org/10.17129/botsci.1875

Refbacks

  • There are currently no refbacks.


ISSN: 2007-4476
Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.