Endogenous sugar level is associated with differential heat tolerance in onion bulb scales
Introduction
Onion (Allium cepa L.), a widespread Alliaceae plant, is one of the main vegetables consumed worldwide. Hot-air curing of bulbs is an important postharvest treatment, used to dry out the outer scales, which are then transformed into a complete skin. This skin protects the bulb from water loss and suppresses disease incidence, thereby maintaining higher quality during storage (Downes et al., 2009; Chope et al., 2012). Application of postharvest heat treatment, 33 °C at 98 % relative humidity (RH) for a few days, to detached outer and inner scales reveals their differential responses to the heat stress (Galsurker et al., 2018). The outer scale desiccates and turns into papery dry skin, while the inner scale exhibits tolerance to the heat stress, maintaining high relative water content (RWC; Galsurker et al., 2018). The mechanism responsible for these scales’ differential heat response is unknown.
Plant tissue copes with heat stress through a series of biochemical and metabolic changes; among these is the accumulation of compatible solutes that help the plant reestablish osmotic homeostasis by increasing the water potential, protecting cellular organelles and stabilizing proteins and membranes (Hasanuzzaman et al., 2013). The accumulated compatible solutes, also termed osmoprotectants, are low-molecular-weight organic solutes that are highly soluble and do not affect plant metabolism (Yancey, 2005). Several soluble sugars are considered osmoprotectants, shown to accumulate in plants in response to abiotic stresses, including high temperature, and to maintain cell homeostasis (Hare et al., 1998; Vinocur and Altman, 2005).
Onion bulbs contain fructose, glucose, sucrose and a series of fructo-oligosaccharides (fructans) as the main non-structural carbohydrates, accounting for 80 % of bulb dry matter (DM; Darbyshire and Henry, 1981; Benkeblia et al., 2004). During bulb storage, metabolic activities lead to quantitative variations in sugar composition which are strongly related to the transition from dormancy to sprouting (Benkeblia and Varoquaux, 2003; Ohanenye et al., 2019). However, there are conflicting reports on the nature of the changes in soluble sugars in onion bulbs during storage. After prolonged storage, a considerable decrease in the amount of fructose and glucose was reported in the equatorial slice of the bulb (Chope et al., 2007). In other studies, fructose levels were reported to increase during the first month of storage but then they decreased (Benkeblia et al., 2002; Benkeblia and Varoquaux, 2003). Downes et al. (2010) reported increase in fructose and glucose levels at the bulb skin of 'Red Baron' and 'Sherpa' during six weeks of curing (20−28 °C) followed by decrease or no change after seven month of cold storage. Wellington cultivar showed an opposite pattern in most glucose and fructose measurements. Although there are many studies describing the sugar alterations during onion bulb storage, the nature of the changes in sugar content is not yet clear and there are no reports evaluating the soluble sugar levels and their functions in different onion scales in the same bulb.
The main aims of this study were to assess the role of soluble sugars in the differential heat response of outer and inner onion bulb scales. We showed that high soluble sugars promote heat tolerance in the inner scale. In the outer scale, on the other hand, we found that sugars are rapidly metabolized to form skin tissue.
Section snippets
Plant materials and heat treatment
Commercial brown onion cv. Orlando was grown in sandy soil in the northwestern Negev desert, Israel, in the years 2015–2017. The onions were not treated with maleic hydrazide before leaf drop, the common agricultural practice, and did not undergo field curing. Onions were harvested manually at 80–100 % fallen leaves (top–down) and the leaves were removed with a sharp knife, leaving a ∼5-cm long neck above the bulb, as described previously (Eshel et al., 2014). Dry muddy skin was removed to
Heat treatment induces different osmolarity profiles in outer vs. inner scales
Our previous study showed that the first outer onion scale dramatically desiccates via loss of RWC during heat treatment, while the fifth inner scales maintain their RWC and are thus termed heat tolerant (Galsurker et al., 2018). To determine the factors that might be involved in the differential heat response, detached outer and inner onion scales were heated at 33 °C and 98 % RH and their osmolarity measured over 6 d. Differential osmolarity levels were found between outer and inner scales
A high level of soluble sugars promotes heat tolerance in the inner scale
Only outer scales of onion can form dry brown skin during heat stress, while the inner scales maintain high water content and do not change color (Galsurker et al., 2018). During heating, osmolarity and hexose levels were reduced in the outer scale, and were stable in the inner one, suggesting their possible involvement in maintaining the osmotic pressure of internal onion scales (Fig. 1). Such high osmotic pressure could have a role in the heat tolerance of the inner scales. The high level of
Conclusions
The differential response of detached outer and inner bulb scales to heat stress suggests the activation of different cascades of events leading to skin formation and viable heat resistance, respectively (Fig. 5). While the inner scales maintained high osmolarity, DM and sugar levels, all of these factors were dramatically reduced in the outer scales. In onion scales, high osmolarity, caused by a high level of soluble sugars in the plant tissue, inhibited water loss. The transcriptome analysis
Author statement
Ortal Galsurker: Investigation, Methodology, Validation, Formal analysis. Gilor Kelly: Methodology, Resources. Adi Doron-Faigenboim: Investigation, Formal analysis. Kalaivani Aruchamy: Data Curation. Bolaji Babajide Salam: Data Curation. Paula Teper-Bamnolker: Resources, Project administration. Amnon Lers: Writing - Review & Editing, Supervision. Dani Eshel: Conceptualization, Writing - Review & Editing, Supervision.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This research was funded by a grant from the Chief Scientist of the Ministry of Agriculture and Rural Development of Israel (no. 430-0416-13). We thank Prof. Menachem Moshelion for fruitful discussions.
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