Water deficit stress (WDS)-tolerance in grain amaranths (Amaranthus hypochondriacus, A. cruentus and A. caudatus), and A. hybridus, their presumed shared ancestor, was examined. A. hypochondriacus was the most WDS-tolerant species, a trait that correlated with an enhanced osmotic adjustment (OA), a stronger expression of abscisic acid (ABA) marker genes and a more robust sugar starvation response (SSR). Superior OA was supported by higher basal hexose (Hex) levels and high Hex/sucrose (Suc) ratios in A. hypochondriacus roots, which were further increased during WDS. This coincided with increased invertase, amylase and sucrose synthase activities and a strong depletion of the starch reserves in leaves and roots. The OA was complemented by the higher accumulation of proline, raffinose, and other probable raffinose-family oligosaccharides of unknown structure in leaves and/or roots. The latter coincided with a stronger expression of Galactinol synthase 1 and Raffinose synthase in leaves. Increased SnRK1 activity and expression levels of the class II AhTPS9 and AhTPS11 trehalose phosphate synthase genes, recognized as part of the SSR network in Arabidopsis, were induced in roots of stressed A. hypochondriacus. It is concluded that these physiological modifications improved WDS in A. hypochondriacus by raising its water use efficiency.

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.

In this study, water deficit stress (WDS)-tolerance in several cultivars of grain amaranth species (Amaranthus hypochondriacus [Ahypo], A. cruentus [Acru] and A. caudatus [Acau]), in addition to A. hybridus (Ahyb), an ancestral amaranth, was examined. Ahypo was the most WDS-tolerant species, whereas Acau and Ahyb were WDS-sensitive. Data revealed that the differential WDS tolerance observed was multifactorial. It involved increased proline and raffinose (Raf) in leaves and/ or roots. Higher foliar Raf coincided with induced Galactinol synthase 1 (AhGolS1) and Raffinose synthase (AhRafS) expression. Unknown compounds, possibly larger RFOs, also accumulated in leaves of WDS-tolerant amaranths, which had high Raf/ Verbascose ratios. Distinct nonstructural carbohydrate (NSC) accumulation patterns were observed in tolerant species under WDS and recovery, such as: i) high Hex/ Suc ratios in roots coupled to increased cell wall and vacuolar invertase and sucrose synthase activities; ii) a severer depletion of starch reserves; iii) lower NSC content in leaves, and iv) higher basal hexose levels in roots which further increased under WDS. WDS-marker gene expression patterns proposed a link between amaranth’s WDS tolerance and abscisic acid-dependent signaling. Results obtained also suggest that AhTRE, AhTPS9, AhTPS11, AhGolS1 and AhRafS are reliable gene markers of WDS tolerance in amaranth.HighlightDifferential water deficit stress tolerance in grain amaranths and their ancestor, Amaranthus hybridus, is a multifactorial process involving various biochemical changes and modified expression patterns of key stress-related genes.