Highest Defoliation Tolerance in Amaranthus cruentus Plants at Panicle Development Is Associated With Sugar Starvation Responses

Abstract

Defoliation tolerance (DT) in Amaranthus cruentus is known to reach its apex at the panicle emergence (PE) phase and to decline to minimal levels at flowering (FL). In this study, defoliation-induced changes were recorded in the content of non-structural carbohydrates and raffinose family oligosaccharides (RFOs), and in the expression and/or activity of sugar starvation response-associated genes in plants defoliated at different vegetative and reproductive stages. This strategy identified sugar-starvation-related factors that explained the opposite DT observed at these key developmental stages. Peak DT at PE was associated with increased cytosolic invertase (CI) activity in all organs and with the extensive induction of various class II trehalose-phosphate synthase (TPS) genes. Contrariwise, least DT at FL coincided with a sharp depletion of starch reserves and with sucrose (Suc) accumulation, in leaves and stems, the latter of which was consistent with very low levels of CI and vacuolar invertase activities that were not further modified by defoliation. Increased Suc suggested growth-inhibiting conditions associated with altered cytosolic Suc-to-hexose ratios in plants defoliated at FL. Augmented cell wall invertase activity in leaves and roots, probably acting in a regulatory rather than hydrolytic role, was also associated with minimal DT observed at FL. The widespread contrast in gene expression patterns in panicles also matched the opposite DT observed at PE and FL. These results reinforce the concept that a localized sugar starvation response caused by C partitioning is crucial for DT in grain amaranth.

Identification of genetic and biochemical mechanisms associated with heat shock and heat stress adaptation in grain amaranths

“…Abiotic stress in grain amaranths: Salt and water deficit stress treatments Five-to six-week-old A. hypochondriacus plants in the vegetative 2 (V2) stage, having 9-15 expanded leaves (Cisneros-Hernańdez et al, 2021) were used to perform water-deficit and salinity stress experiments, which were performed in the growth room conditions mentioned above. Ten to twelve plants per stress treatment were employed and each treatment was replicated twice.…”

“…They also sustain severe defoliation, insect and/or pathogen damage and thrive in poor soils and low-input agricultural systems. This resilience has been associated with various anatomical, physiological and biochemical adaptations ( 2014 ; 2015 ; Miller et al., 1984 ; Lal and Edwards, 1996 ; Brenner et al., 2000 ; Johnson and Henderson, 2002 ; Délano-Frier et al., 2004 ; Liu and Stützel, 2004 ; Sánchez-Hernández et al., 2004 ; Omami and Hammes, 2006 ; Omamt et al., 2006 ; Aguilar-Hernández et al., 2011 ; Huerta-Ocampo et al., 2011 ; Caselato-Sousa and Amaya-Farfán, 2012 ; Castrillón-Arbeláez et al., 2012 ; Vargas-Ortiz et al., 2013 ; Vargas-Ortiz et al, 2015 ; Casarrubias-Castillo et al., 2014 ; González-Rodríguez et al., 2019 ; Jamalluddin et al., 2019 ; Cisneros-Hernández et al., 2021 ). Additional data from a large-scale transcriptomic analysis of A. hypochondriacus plants revealed the presence several orphan or unknown function genes that changed their expression levels in response to diverse stress conditions ( Délano-Frier et al., 2011 ), a number of which were found to significantly increase (a)biotic stress tolerance when over-expressed in Arabidopsis thaliana ( Massange-Sánchez et al, 2015 ; Massange-Sánchez et al, 2016 ; Palmeros-Suárez et al, 2015 ; Palmeros-Suárez et al, 2017 ; Cabrales-Orona, 2016 ; Cabrales-Orona, 2017 ; Cabrales-Orona, 2016 ; Cabrales-Orona, 2017 ; Cabrales-Orona and Délano-Frier, 2021 ; Cabrales-Orona et al., 2022 ).…”

Functional Characterization of an Amaranth Natterin-4-Like-1 Gene in Arabidopsis thaliana

“…Defoliation treatments were performed using A. cruentus plants cv. "Tarasca" as described before by Vargas-Ortiz et al (2015) and Cisneros-Hernández et al (2021). The choice of the "Tarasca" cultivar reflected its previous use as the model plant for ample defoliation-related research in grain amaranth (Castrillón-Arbeláez et al, 2012;Vargas-Ortiz et al, 2013.…”

“…Measurement of Physiological and Biochemical Parameters: Soluble and Insoluble NSCs, Proline, Total Phenols and Flavonols, Catalase and Superoxide Dismutase Enzyme Activities Soluble (i.e., glucose [Glc], fructose [Fru] and sucrose [Suc]) and insoluble (i.e., starch) NSC contents in lyophilized ground tissues were determined enzymatically using a coupled assay as described previously (Cisneros-Hernández et al, 2021). Proline was assayed colorimetrically, at 520 nm, via the measurement of the red chromogen produced by its reaction with ninhydrin at low pH (Bates et al, 1973).…”

“…Grain amaranths are considered stress-tolerant species that can readily adapt to drought, severe defoliation and poor soils (Caselato-Sousa and Amaya-Farfán, 2012;Castrillón-Arbeláez et al, 2012;Vargas-Ortiz et al, 2013. This trait has been associated with various anatomical, physiological and biochemical adaptations (Miller et al, 1984;Lal and Edwards, 1996;Johnson and Henderson, 2002;Omamt et al, 2006;Aguilar-Hernández et al, 2011;Huerta-Ocampo et al, 2011González-Rodríguez et al, 2019;Cisneros-Hernández et al, 2021). Additionally, grain amaranths are generally known to be tolerant to insect pests and pathogens (Brenner et al, 2000;Délano-Frier et al, 2004;Sánchez-Hernandez et al, 2004;Casarrubias-Castillo et al, 2014).…”