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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Biochemical and physiological time-of-day variations in early-development phase of Agave mapisaga and Agave salmiana

Jesus A. Jiménez-Torres https://orcid.org/0000-0001-6231-6172 A , Cecilia B. Peña-Valdivia https://orcid.org/0000-0003-4245-0547 A * , Baruch Arroyo A , Daniel Padilla-Chacón https://orcid.org/0000-0001-9887-1063 A and Rodolfo García A
+ Author Affiliations
- Author Affiliations

A Programa de Posgrado en Botánica, Colegio de Postgraduados, Carretera México-Texcoco km 36.5, Montecillo, Estado de México 56264, Mexico.

* Correspondence to: cecilia@colpos.mx

Handling Editor: Thomas Roberts

Functional Plant Biology 51, FP23244 https://doi.org/10.1071/FP23244
Submitted: 5 January 2023  Accepted: 4 August 2024  Published: 29 August 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

This research assesses the aboveground matter accumulation and Fv/Fm ratios (maximum quantum efficiency of PSII) in young plants (5 months old) of Agave mapisaga and Agave salmiana grown under greenhouse conditions. This study also evaluated changes in the relative abundance of several different metabolites (sugars, free amino acids, and soluble phenols) during the major daily phases (I, III, and IV) of Crassulacean acid metabolism (CAM). These two species were also investigated to determine if differences in these parameters were evident with respect to their geographical origins (i.e. Metepec, Tlajomulco, and Tlaxiaca, in the state of Hidalgo, Mexico). Differences in shoot mass (0.51−0.82 g plant−1), water content (75−93%), fructose (4−27 μmol g−1), glucose (57−73 μmol g−1), sucrose (10−30 μmol g−1), free amino acids (5−25 μmol g−1), soluble phenolics (0.7−3.5 μmol g−1), and Fv/Fm ratios (0.75−0.80) were evident between plants with different origins. Specifically, at the end of Phase I compared to Phase IV, the results showed significant reductions in dry matter (up to 3.3%) and also reductions in fructose/sucrose. Relative amino acid concentrations were lowest in Phase III (8.8 μmol g−1) compared to Phase I (16 μmol g−1). These are novel observations, since all these changes and the biochemical and physiological performance in the CAM phases have not been previously determined in Agave plants differing in their geographical origins.

Keywords: Agave, CAM phases, carbon metabolism, free amino acids, Fv/Fm, maguey, seed provenance, soluble sugars.

References

Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytologist 186, 786-793.
| Crossref | Google Scholar |

Almaraz-Abarca N, Delgado-Alvarado EA, Ávila-Reyes JA, Uribe-Soto JN, González-Valdez LS (2013) The phenols of the genus Agave (Agavaceae). Journal of Biomaterials and Nanobiotechnology 4, 9-16.
| Crossref | Google Scholar |

Anderies JM, Nelson BA, Kinzig AP (2008) Analyzing the impact of Agave cultivation on famine risk arid pre-Hispanic northern Mexico. Human Ecology 36, 409-422.
| Crossref | Google Scholar |

Antony E, Borland AM (2009) The role and regulation of sugar transporters in plants with Crassulacean acid metabolism. In ‘Progress in botany’. (Eds U Lüttge, W Beyschlag, B Büdel, D Francis) pp. 127–143 (Springer: Berlin, Germany) doi:10.1007/978-3-540-68421-3_6

Aragón-Gastélum JL, Ramírez-Benítez JE, González-Durán E, González-Salvatierra C, Ramírez-Tobías HM, Flores J, Gutiérrez-Alcántara EJ, Méndez-Guzmán E, Jarquín-Gálvez R (2020) Photochemical activity in early-developmental phases of Agave angustifolia subsp. tequilana under induced global warming: implications to temperature stress and tolerance. Flora 263, 151535.
| Crossref | Google Scholar |

Ashraf MA, Iqbal M, Rasheed R, Hussain I, Riaz M, Arif MS (2018) Environmental stress and secondary metabolites in plants. In ‘Plant metabolites and regulation under environmental stress’. (Eds P Ahmad, MA Ahanger, VP Singh, DK Tripathi, P Alam, MN Alyemeni) pp. 153–167. (Academic Press) doi:10.1016/B978-0-12-812689-9.00008-X

Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Research 5(F1000 Faculty Rev), 1554.
| Crossref | Google Scholar |

Borland AM, Guo HB, Yang X, Cushman JC (2016) Orchestration of carbohydrate processing for crassulacean acid metabolism. Current Opinion in Plant Biology 31, 118-124.
| Crossref | Google Scholar |

Bräutigam A, Schlüter U, Eisenhut M, Gowik U (2017) On the evolutionary origin of CAM photosynthesis. Plant Physiology 174, 473-477.
| Crossref | Google Scholar |

Ceusters J, Borland AM, Taybi T, Frans M, Godts C, De Proft MP (2014) Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism. Journal of Experimental Botany 65, 3705-3714.
| Crossref | Google Scholar |

CONAGUA (2020) Normal weather information 1981–2010 of Hidalgo state climatic stations. Available at https://smn.conagua.gob.mx/es/informacion-climatologica-por-estado?estado=hgo

Delgado-Alvarado EA, Ávila-Reyes JA, Torres-Ricario R, Naranjo-Jiménez N, Chaidez-Ayala AI, Almaraz-Abarca N (2021) Caracterización fitoquímica de Agave shrevei Gentry. ECUCBA 8, 56-59.
| Crossref | Google Scholar |

Dincheva I, Badjakov I, Galunska B (2023) New insights into the research of bioactive compounds from plant origins with nutraceutical and pharmaceutical potential. Plants 12, 258.
| Crossref | Google Scholar |

Fondom NY, Castro-Nava S, Huerta AJ (2009) Photoprotective mechanisms during leaf ontogeny: cuticular development and anthocyanin deposition in two morphs of Agave striata that differ in leaf colouration. Botany 87, 1186-1197.
| Crossref | Google Scholar |

Gouws LM, Osmond CB, Schurr U, Walter A (2005) Distinctive diel growth cycles in leaves and cladodes of CAM plants: differences from C3 plants and putative interactions with substrate availability, turgor and cytoplasmic pH. Functional Plant Biology 32, 421-428.
| Crossref | Google Scholar |

Hildebrandt TM (2018) Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Molecular Biology 98, 121-135.
| Crossref | Google Scholar |

Jiménez-Torres JA, Peña-Valdivia CB, Padilla-Chacón D, García-Nava R (2021) Physiological and biochemical responses of Agave to temperature and climate of their native environment. Flora 278, 151797.
| Crossref | Google Scholar |

Jones DL, Owen AG, Farrar JF (2002) Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biology and Biochemistry 34, 1893-1902.
| Crossref | Google Scholar |

Júdez L (1989) Técnicas de análisis de datos multidimensionales. MAPA. Madrid, 301 pp.

Kaur G, Ganjewala D (2019) Stress protectant secondary metabolites and their metabolic engineering to enhance abiotic stress tolerance in plants. In ‘In vitro plant breeding towards novel agronomic traits’. (Eds M Kumar, A Muthusany, V Kumar, N Bhalla-Sarin) pp. 197–216 (Springer: Berlin, Germany)

Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63, 1593-1608.
| Crossref | Google Scholar |

Livingston DP, III, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences 66, 2007-2023.
| Crossref | Google Scholar |

López-Navarrete MC, Peña-Valdivia CB, Trejo C, Padilla-Chacón D, García N R, Martínez B E (2021) Interaction among species, time-of-day, and soil water potential on biochemical and physiological characteristics of cladodes of Opuntia. Plant Physiology and Biochemistry 162, 185-195.
| Crossref | Google Scholar |

Lüttge U (2004) Ecophysiology of Crassulacean acid metabolism (CAM). Annals of Botany 93, 629-652.
| Crossref | Google Scholar |

Magalhães LM, Santos F, Segundo MA, Reis S, Lima JLFC (2010) Rapid microplate high-throughput methodology for assessment of Folin-Ciocalteu reducing capacity. Talanta 83, 441-447.
| Crossref | Google Scholar |

Mellado-Mojica E, Gonzáles de la Vara LE, López MG (2017) Fructan active enzymes (FAZY) activities and biosynthesis of fructooligosaccharides in the vacuoles of Agave tequilana Weber Blue variety plants of different age. Planta 245, 265-281.
| Crossref | Google Scholar |

Mora-López LJ, Reyes-Agüero AJ, Flores-Flores LJ, Peña-Valdivia CB, Aguirre-Rivera RJ (2011) Morphological variation and humanization of Agave genus, Salmianae section. Agrociencia 45, 465-477.
| Google Scholar |

Morejón R, Díaz SH (2005) Análisis de asociación de caracteres en el cultivo de arroz (Oryza sativa L.) empleando técnicas multivariadas. Cultivos Tropicales 26(1), 77-81.
| Google Scholar |

Niechayev NA, Jones AM, Rosenthal DM, Davis SC (2019) A model of environmental limitations on production of Agave americana L. grown as a biofuel crop in semi-arid regions. Journal of Experimental Botany 70, 6549-6559.
| Crossref | Google Scholar |

Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Biology 29, 379-414.
| Crossref | Google Scholar |

Peña-Valdivia CB, Ortega-Delgado ML (1991) Non-structural carbohydrate partitioning in Phaseolus vulgaris after vegetative growth. Journal of the Science of Food and Agriculture 55, 563-577.
| Crossref | Google Scholar |

Pimienta-Barrios E, Robles-Murguia C, Nobel PS (2001) Net CO2 uptake for Agave tequilana in a warm and a temperate environment. Biotropica 33, 312-318.
| Crossref | Google Scholar |

Puente-Garza CA, Gutiérrez-Mora A, García-Lara S (2015) Micropropagation of Agave salmiana: means to production of antioxidant and bioactive principles. Frontiers in Plant Science 6, 1026.
| Crossref | Google Scholar |

R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/

Ramírez-Tobías HM, Peña-Valdivia CB, Trejo C, Aguirre RJR, Vaquera HH (2014) Seed germination of Agave species as influenced by substrate water potential. Biological Research 47, 11.
| Crossref | Google Scholar |

Rangel-Landa S, Casas A, Dávila P (2015) Facilitation of Agave potatorum: an ecological approach for assisted population recovery. Forest Ecology and Management 347, 57-74.
| Crossref | Google Scholar |

Reyes-Agüero JA, Peña-Valdivia CB, Aguirre-Rivera JR, Mora-López JL (2019) Infraspecific variation of Agave mapisaga Trel. and A. salmiana Otto ex Salm-Dyck. (Asparagaceae) related to ancestral usages at the Hñähñu region in central Mexico. Agrociencia 53, 563-579.
| Google Scholar |

Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defence pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683-1696.
| Crossref | Google Scholar |

Salinas ML, Ogura T, Soffchi L (2001) Irritant contact dermatitis caused by needle-like calcium oxalate crystals, raphides, in Agave tequilana among workers in tequila distilleries and agave plantations. Contact Dermatitis 44, 94-96.
| Crossref | Google Scholar |

Stewart JR (2015) Agave as a model CAM crop system for a warming and drying world. Frontiers in Plant Science 6, 684.
| Crossref | Google Scholar |

Wickham H (2009) ‘ggplot2: elegant graphics for data analysis.’ (Springer: New York, NY, USA)

Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiologia Plantarum 159, 290-312.
| Crossref | Google Scholar |

Zhang H, Sonnewald U (2017) Differences and commonalities of plant responses to single and combined stresses. The Plant Journal 90, 839-855.
| Crossref | Google Scholar |