Roots of the Resurrection Plant Tripogon loliiformis Survive Desiccation Without the Activation of Autophagy Pathways by Maintaining Energy Reserves

Abstract

Being sessile, plants must regulate energy balance, potentially via source-sink relations, to compromise growth with survival in stressful conditions. Crops are sensitive, possibly because they allocate their energy resources toward growth and yield rather than stress tolerance. In contrast, resurrection plants tightly regulate sugar metabolism and use a series of physiological adaptations to suppress cell death in their vegetative tissue to regain full metabolic capacity from a desiccated state within 72 h of watering. Previously, we showed that shoots of the resurrection plant Tripogon loliiformis , initiate autophagy upon dehydration as one strategy to reinstate homeostasis and suppress cell death. Here, we describe the relationship between energy status, sugar metabolism, trehalose-mediated activation of autophagy pathways and investigate whether shoots and roots utilize similar desiccation tolerance strategies. We show that despite containing high levels of trehalose, dehydrated Tripogon roots do not display elevated activation of autophagy pathways. Using targeted and non-targeted metabolomics, transmission electron microscopy (TEM) and transcriptomics we show that T. loliiformis engages a strategy similar to the long-term drought responses of sensitive plants and continues to use the roots as a sink even during sustained stress. Dehydrating T. loliiformis roots contained more sucrose and trehalose-6-phosphate compared to shoots at an equivalent water content. The increased resources in the roots provides sufficient energy to cope with stress and thus autophagy is not required. These results were confirmed by the absence of autophagosomes in roots by TEM. Upregulation of sweet genes in both shoots and roots show transcriptional regulation of sucrose translocation from leaves to roots and within roots during dehydration. Differences in the cell’s metabolic status caused starkly different cell death responses between shoots and roots. These findings show how shoots and roots utilize different stress response strategies and may provide candidate targets that can be used as tools for the improvement of stress tolerance in crops.

Desiccation-Driven Senescence in the Resurrection Plant Xerophyta schlechteri (Baker) N.L. Menezes: Comparison of Anatomical, Ultrastructural, and Metabolic Responses Between Senescent and Non-Senescent Tissues

“…The significant increase in trehalose during the first 48 h could again suggest operation of the Suc-Tre6P nexus, this possibly regulating sucrose content until photosynthetic competence is gained. Alternatively, it is possible that here trehalose is playing a role in autophagy, allowing clean up of subcellular damage or macromolecular aggregates that may have formed during desiccation and quiescence (Williams et al, 2015; Asami et al, 2019).…”

Stachyose triggers apoptotic like cell death in drought sensitive but not resilient plants

“…Autophagy, another form of cell death is antagonistic to apoptosis. Previously, we showed that trehalose treatment induces the formation of autophagosomes, even in hydrated T. loliiformis leaves 18 , 19 . To determine whether T. loliiformis suppresses stachyose-mediated apoptosis, we infiltrated T. loliiformis leaves with stachyose and KOX and looked for the presence of DNA laddering.…”

“…Conversely, at least some resurrection plants accumulate stachyose in vegetative tissues 16 , 17 . To determine whether stachyose accumulates in drying and desiccated T. loliiformis shoots, we analysed the T. loliiformis transcriptome and metabolome for increased accumulation of stachyose synthase, the enzyme that catalyses the synthesis of stachyose, transcripts and stachyose respectively 18 , 19 . The transcriptome data coupled with RT-PCR showed that dehydrating T.loliiformis shoots accumulate stachyose synthase transcripts (Table 1 ).…”

“…One strategy that helps resurrection plants survive desiccation is transcriptional and metabolic priming in the hydrated state to enable rapid responses to stress. The early onset of dehydration adaptive strategies like autophagy may facilitate desiccation tolerance 19 , 43 . The cell cycle also plays a vital role in growth and development and is driven by energy metabolism 40 , 44 – 46 .…”

Vegetative desiccation tolerance in Eragrostiella brachyphylla: biochemical and physiological responses

“…Proline is a proteinogenic multifunctional amino acid and is essential for primary metabolism and acts as a compatible solute ( Szabados & Savouré, 2010 ). Numerous studies have shown that the proline content in resurrection plants increases under desiccation stress and the examples include Eragrostis nindensis ( Vander Willigen, 2004 ), Selaginella bryopteris ( Pandey et al, 2010 ), Selaginella tamariscina ( Wang et al, 2010 ), Paraisometrum mileense ( Li et al, 2014 ), Sprobolus stapfianus ( Martinelli et al, 2007 ), Tripogonlo liiformis ( Asami et al, 2019 ), Craterostigma wilmsii, Myrothamnus flabellifolius, Xerophyta humilis and viscosa ( Vicré et al, 2004 ). It is crucial in mechanically stabilising the cells and membranes in the desiccated state ( Pandey et al, 2010 ; Vander Willigen, 2004 ).…”