Elsevier

Plant Science

Volume 271, June 2018, Pages 62-66
Plant Science

Review
Saving for a rainy day: Control of energy needs in resurrection plants

https://doi.org/10.1016/j.plantsci.2018.03.009Get rights and content

Highlights

  • Resurrection plants balance their energy needs for growth and development with repair, defence and survival.

  • Energy metabolism, cell cycle and programmed cell death pathways play key roles in desiccation tolerance.

  • High sucrose/glucose ratios activate cytoprotective pathways.

  • Cells do not die from stress but rather from an energy deficit that prevents them from responding effectively.

Abstract

Plants constantly respond to threats in their environment by balancing their energy needs with growth, defence and survival. Some plants such as the small group of resilient angiosperms, the resurrection plants, do this better than most. Resurrection plants possess the capacity to tolerate desiccation in vegetative tissue and upon watering, regain full metabolic capacity within 72 h. Knowledge of how these plants survive such extremes has advanced in the last few decades, but the molecular mechanics remain elusive. Energy and water metabolism, cell cycle control, growth, senescence and cell death all play key roles in resurrection plant stress tolerance. Some resurrection plants suppress growth to improve energy efficiency and survival while sensitive species exhaust energy resources rapidly, have a diminished capacity to respond and die. How do the stress and energy metabolism responses employed by resurrection plants differ to those used by sensitive plants? In this perspective, we summarise recent findings defining the relationships between energy metabolism, stress tolerance and programmed cell death and speculate important roles for this regulation in resurrection plants. If we want to harness the strategies of resurrection plants for crop improvement, first we must understand the processes that underpin energy metabolism during growth and stress.

Introduction

We save because we cannot predict the future. Anon

All organisms face the daily challenge of balancing their energy expenditure between inputs [1]. In animals, this occurs between meals; in plants, this occurs at night and during stress. How well the organism regulates its energy balance, particularly when stressed, dictates its ability to elicit an appropriate response and survive [2]. In addition to stress, cells and proteins undergo routine wear and tear and require repair to maintain homeostasis. Cellular repair is an energy consuming process and the levels of repair rise during stress [[3], [4]]. If the energy reserves available are insufficient to support an appropriate response, the organism may be willing but unable to repair the damage. At least some times, cells, and organisms, do not die from stress directly but rather from an energy deficit that prevents execution of the stress response [4]. One group of plants, the resurrection plants, have the capacity to withstand desiccation to an air-dry state and do not suffer the same fate as the majority of land plants. Although research has made significant progress, the mechanics underpinning the tolerance displayed by resurrection plants remains elusive. Putative explanations towards resurrection plant tolerance include; i) to the ability to slow their metabolism to a quiescent state during drying, ii) the production of copious amounts of osmolytes in the hydrated state that play cytoprotective roles and help control the rate of drying, iii) an ability to protect the cells from damaging UV rays by minimising surface area or disassembling the photosynthetic machinery while still producing enough energy to repair damage, iv) The use of an alternative energy metabolism system that is not utilised in sensitive plants v) a more efficient cellular repair system, vi) the ability to shut down cell death pathways, vii) A combination of all of the above. Here we speculate possible answers to these theories by highlighting the relationships between energy metabolism, desiccation tolerance and cell death in resurrection plants.

Sensitive and tolerant plant species employ stress responses that prevent damage and enhance survival, however, the strategies used and the outcomes produced are starkly different. Sensitive species can tolerate water losses of up to 40% relative water content (RWC). Desiccation tolerant plants on the other hand can survive losses of up to 95% of their RWC and are categorised into two classes, fully desiccation tolerant and modified desiccation tolerant, depending on the rate of drying tolerated [5,6]. Fully-desiccation tolerant plants, also known as constitutively desiccation tolerant plants, include non-vascular species such as mosses and bryophytes, can survive drying at any rate and utilise extensive repair mechanisms for tolerance [7]. In contrast, the vascular modified desiccation tolerant plants cannot tolerate rapid drying and thus employ control mechanisms that slow down the rate of water loss [5].

In contrast to sensitive species, modified desiccation tolerant plants such as resurrection plants use excess energy produced in the hydrated state to generate dehydration-associated metabolites [8]. Potentially, this enables them to be significantly more energy efficient and subsequently stress tolerant. By producing osmoprotectants in the hydrated state, resurrection plants can focus their limited energy resources during drying towards cell repair and cytoprotection [9].

A universal response to water deficit in plants is stomatal closure and the subsequent shutdown of photosynthesis. In resurrection plants, this shutdown occurs rapidly, upon water losses as little as 20–30% RWC [10]. For example, the photosynthetic rate of Tripogon loliiformis is reduced by 20% at 90% RWC and further declined to 50% when the RWC drop to 80%; at 70% RWC no photosynthesis was detected (Fig. 1)[11]. Conversely, many of the faster growing sensitive plants continue to photosynthesise, albeit inefficiently, until much lower relative water contents when it is too late to respond. In modified resurrection plants, the early shutdown of photosynthesis can promote survival. These plants cannot tolerate rapid drying, thus the rapid closure of stomata supports survival by providing additional time for the plant to employ adaptive measures. Once the plant has prepared for desiccation, water is rapidly lost from the 60–<30% RWC stages. Fully-desiccation tolerant plants also shutdown photosynthesis, however, not as rapidly. Studies in the moss Polytrichum formosum demonstrated active photosynthesis until 40% RWC [12] The rapid photosynthetic shutdown and production of osmoprotectants in the hydrated state causes resurrection plants to grow slower than their sensitive counterparts [6]. This slow growth reduces their metabolic requirements and allows resurrection plants to maintain a tighter control of the dehydration of their vegetative tissue [6]. The compensation of cellular metabolic status and growth rate with minimised water loss is just one of the mechanisms employed by the T.loliiformis to tolerate desiccation.

In addition to controlling the rate of water loss, resurrection plants typically couple photosynthetic shutdown with a myriad of physiological and metabolic changes that protect the photosynthetic machinery and minimise damage [[8], [9]]. Thus, the cells in resurrection plant vegetative tissue may not undergo as much damage from running an inefficient photosynthesis system compared to those present in sensitive species. Despite these advantages, the early shutdown of photosynthesis leads to caloric deficiency and energy deficit, which if left unchecked can lead to an inability to mount a stress response. To survive, resurrection plants must tap into alternative energy sources as well as reduce energy expenditure.

In addition to serving as fuels for metabolism, sugars act as primary messengers for the regulation of plant growth and stress responses. With their different growth rates, it is apparent that sensitive species and resurrection plants utilise their metabolic resources differently. A key feature of many resurrection plants upon dehydration is the metabolic shift to sucrose and amino acid biosynthesis. This shift is sufficient to meet the cell’s needs but also results in the creation of high sucrose/glucose ratios that trigger significant changes to the cell’s metabolism [[13], [14]]. Amongst other signals such as hormones and the available nitrogen content, the cell uses the ratio of sucrose/hexoses to help direct the metabolic status of the cell. High sucrose/low glucose ratios indicate a cellular energy imbalance, to help maintain homeostasis the cell directs its cell’s metabolism towards cytoprotection rather than growth. Accordingly, leaves infiltrated with sucrose display increased expression of redox regulators, transcription factors including members of the NAC (NAP), MYB (AtMYB14, MYB90), bZIP (AtbZIP9 and 11) and WRKY (WKRY 26, 53 and 75) associated with energy metabolism as well as proteasome-mediated degradation, trehalose metabolism and autophagy [15] (Fig. 2). It is feasible that in resurrection plants, the high sucrose/glucose ratios created upon dehydration allow the plant to slow-down growth related activities and focus energy resources towards survival. For example, increased sugar levels upon dehydration of the resurrection grass Sporobolus stapfianus act as a signal to slow down cellular metabolism and trigger cytoprotective pathways[16].

Hormone signalling is an integral component of plant defence, responses to the environment and regulation of senescence and as such is expected to play a significant role in the desiccation tolerance mechanisms of resurrection plants. To date, however only limited studies have been performed [17,18]. During early drying, plants accumulate Abscissic Acid (ABA) to trigger the transcription of protective proteins and acts as a signal for the plant to initiate adaptive responses to water deficit [19,20]. Plant hormones may also play a role in the ability of resurrection plants to suppress senescence. In particular, Auxins, ethylene, ABA, salicylic acid (SA) and jasmonic acid (JA) have all been linked to senescence and cell death regulation [21,22,23]. The role that these hormones play in the regulation of cell death in resurrection plants remains unclear and should remain a focus of current and future research [24,25].

The cell’s pre-existing proteome may serve as an alternative energy reserve that is released by protein turnover and autophagy when energy reserves levels are low. Autophagy is an intracellular process that remobilises bulk cytoplasmic material in double-membraned vesicles termed autophagosomes for degradation and recycling [26]. A double-edged sword, autophagy promotes survival, however, if too much autophagy occurs cells can die with autophagic features. The balance of cellular autophagy is therefore tightly regulated by the metabolite sensors, mechanistic target of rapamycin (mTOR) and the Sucrose non-fermenting 1–related kinase 1 (SnRK1) [27]. When energy is present, via nitrogen and carbon availability, mTOR suppresses autophagy and promotes anabolism and growth. Conversely, SnKR1 regulates cellular nutrient status to drive catabolism and autophagy during energy deficit [26]. Specifically, SnRK1 regulates carbohydrate metabolism via transcriptional modulation of genes involved in sucrose and starch degradation. Once broken down, these sugars drive the flow of carbon through glycolysis and the tricarboxylic acid (TCA) cycle leading to accumulation of TCA cycle intermediates and glucose-6-phosphate [21]. Recent studies in our lab showed that trehalose triggers autophagy via induction of SnRK1 [21]. Trehalose is an established promoter of desiccation tolerance and generated from glucose via trehalose-6-phosphate (T6P). When glucose levels drop, the cell cannot synthesise as much T6P. Simultaneously, Trehlaose-6-phosphate phosphatase (T6PP) converts the present T6P to trehalose resulting in high trehalose/T6P ratios. High trehalose/T6P ratios coincide with high sucrose/glucose ratios and are indicative of energy deficit and induce activity of the metabolic regulator SnRK1 [[28], [29]]. Additionally, trehalose blocks glucose metabolism thus further biasing the cell towards a high trehalose/T6P ratio. In contrast, high cellular glucose levels lead to a low trehalose/T6P ratio and are indicative of energy sufficiency. Energy sufficiency, specifically T6P, triggers mTOR to suppress SnRK1 (Fig. 3).

The default response of an organism is to survive. Although seemingly counterintuitive, if stress is severe or prolonged the organism will elicit altruistic death of select cells for the greater good of the organism [30,31]. Autophagy is triggered during the dehydration of both tolerant and sensitive species, thus the induction of autophagy alone does not provide desiccation tolerance. How do sensitive and tolerant species regulate autophagy; and do tolerant species regulate autophagy pathways more effectively?

During dehydration the Australian resurrection plant, Tripogon loliiformis, uses trehalose to activate autophagy and reinstate cellular homeostasis [30]. The exogenous application of trehalose activates autophagy in both Tripogon and Arabidopsis leaves. This suggests that Arabidopsis and Tripogon contain similar autophagy pathways, at least in response to trehalose. Unlike Tripogon, however, Arabidopsis does not produce significant amounts of trehalose during drought. Thus, sensitive and tolerant species may encode similar autophagy pathways but at least some resurrection plants use unique metabolic stimuli such as trehalose to enable them to regulate autophagy more effectively.

How important is autophagy for desiccation tolerance and do all resurrection plants use autophagy pathways as a conserved desiccation tolerance strategy? At first glance, it appears the induction of autophagy is not universal for desiccation tolerance. In fact, recent studies suggest that the requirement for autophagy may depend on the desiccation tolerance strategies of the resurrection plant [7,32]. Resurrection plants are classified into two major groups depending on whether they maintain (homeochlorophyllous) or disassemble (poikilochlorophyllous) their photosynthetic apparatus during desiccation.

Rubisco (D-ribulose-1,5-bisphosphate carboxylase/oxgensase) is a major component of the photosynthesis CO2 assimilation system and is the most abundant protein in the world [33]. In terms of a plant cell, rubisco represents 20–30% of total leaf nitrogen in C3 plants and 30% of soluble protein in C4 plants [34]. Tripogon loliiformis and Boea hygrometrica, are homiochlorophyllus resurrection plants that retain their chlorophyll during dehydration and therefore trigger autophagy to release nitrogen [30,35]. In contrast, Xerophyta viscosa, is a poikilochlorophyllus resurrection plant and possibly degrades significant amounts of rubisco during dehydration to provide copious amounts of available nitrogen [5]. This increased availability of nitrogen may lessen the role for autophagy in some species. Instead, poikilochlorophyllus plants such as X.viscosa may rely on more subtle measures such as proteosomal protein degradation in addition to autophagy to provide their energy stores. Consistent with this hypothesis, transcriptome analysis of X.viscosa did not reveal induction of autophagy but rather demonstrated significant increases in transcripts associated with the unfolded protein response and protein turnover [36]. Furthermore, the increased production of reactive oxygen species in homeochlorophyllous resurrection plants can also trigger autophagy during dehydration. Overall, it appears that autophagy does facilitate desiccation tolerance, however, whether it is essential depends on the metabolism of the organism.

Cell cycle status is regulated by sugar and energy metabolism and may have significant effects on cell death outcomes in animals and plants [16,37]. In animals, apoptosis occurs preferentially in proliferating cells [37]. Furthermore, metabolites present in late G1 phase are required for cell death [38,39]. Similar studies using synchronised BY-2 tobacco cells showed that cryptogein, a proteinaceous elicitor of cell death, induced ROS production in all cell cycle phases but could only initiate cell death in the G1 and S-phases [40]. Contrastingly, cadmium application caused cell death in both G1 and G2 phases, however, only the G2 phase displayed features associated with apoptotic-like cell death [41]. The specific induction of apoptotic-like cell death in the G2 phase is intriguing and may be driven by sugar metabolism [42]. Glucose signals initiate G2/M transition in meristematic cells by activating the major cell cycle components required for this process [43]. Reduced sucrose and the subsequent drop in the sucrose/glucose ratio may cause cells to progress to the G2 phase where they are susceptible to apoptotic-like cell death signals. Additionally, high glucose levels promote starch breakdown and respiration, which lead to senescence and nutrient recycling to release energy stores [44]. Accordingly, Arabidopsis leaves treated with glucose display accelerated leaf yellowing and developmental senescence [45]. Based on these observations it is reasonable to speculate that some of the selective senescence observed in specific resurrection plant tissues during drying may be due to increased glucose levels and respiration as well as changes to the cell cycle. Additionally, a shift in metabolism during desiccation may potentially play a role in cell cycle regulation hence prevent cell death.

Over the years, conventional breeding programmes have led to the development of crops that metabolise rapidly and produce high grain yields. Although desirable for modern agriculture, these traits come at a metabolic and physiological cost. The rapid growth of crop plants requires significant energy expenditure that leaves little behind for stress responses when required. We suggest that the fundamental energy systems driving the metabolism of resilient species not only enable the organism to respond to stress but to do so in an energy and water efficient manner. Sensitive plants have similar fundamental systems to resilient plants but not the regulatory finesse to utilise their energy resources as effectively. This has wide-spanning implications and effects the organism’s capacity to grow and tolerate stress. Future work should focus on characterising differences in the energy signalling of sensitive and tolerant species, specifically the regulatory targets used by each species. Resilient species such as resurrection plants are geared towards survival not yield, as such translating all key metabolic regulating mechanisms used by resilient species to crops is undesirable. If resurrection plants are to be used for the improvement of agronomic crops then a compromise between growth, tolerance and yield must be identified. Future work should focus on deciphering the role of energy metabolism in resurrection plant tolerance. Once elucidated, educated decisions can be made on how survival strategies from this fascinating group of plants can be best used to improve crop tolerance.

Section snippets

Acknowledgements

This work was supported by a QUT student scholarship (P.A.), professional capacity development grant (S.M) and a QUT Vice Chancellor’s Research Fellowship (B.W).

References (45)

  • P.M. Hasegawa

    Sodium (Na+) homeostasis and salt tolerance of plants

    Environ. Exp. Bot.

    (2013)
  • M. Nietzsche et al.

    A protein–protein interaction network linking the energy-sensor kinase SnRK1 to multiple signaling pathways in Arabidopsis thaliana

    Curr. Plant Biol.

    (2016)
  • J. Kim et al.

    To grow old: regulatory role of ethylene and jasmonic acid in senescence

    Front. Plant Sci.

    (2015)
  • Vesna Dragičević

    Thermodynamics of abiotic stress and stress tolerance of cultivated plants

    Recent Advances in Thermo and Fluid Dynamics

    (2017)
  • M.S. Hossain et al.

    Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress

    Front. Plant Sci.

    (2016)
  • V. Ambastha et al.

    Programmed cell death in plants: a chloroplastic connection

    Plant Signal. Behav.

    (2015)
  • J.M. Farrant

    A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker)

    Planta

    (2015)
  • D. Challabathula et al.

    Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants

    Ann. N. Y. Acad. Sci.

    (2016)
  • C. Dinakar et al.

    Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis

    Front. Plant Sci.

    (2013)
  • K. Urano et al.

    Analysis of plant hormone profiles in response to moderatedehydration stress.pdf

    Plant J.

    (2017)
  • J.M. Farrant

    A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker)

    Planta

    (2015)
  • T. Tan

    Efficient modulation of photosynthetic apparatus confers desiccation tolerance in the resurrection plant Boea hygrometrica

    Plant Cell Physiol.

    (2017)
  • M.R. Karbaschi et al.

    Tripogon loliiformis elicits a rapid physiological and structural response to dehydration for desiccation tolerance

    Funct. Plant Biol.

    (2016)
  • C.F. Michael Proctor et al.

    Desiccation; tolerance in the moss polytrichum formosum: physiological and fine-structural changes during desiccation and recovery desiccation tolerance in the moss polytrichum formosum: physiological and fine-structural changes during desiccation and Re

    Ann. Bot.

    (2007)
  • C. Ma

    Transcriptomic analysis reveals numerous diverse protein kinases and transcription factors involved in desiccation tolerance in the resurrection plant Myrothamnus flabellifolia

    Hortic. Res.

    (2015)
  • Q. Zhang et al.

    The role of transketolase and octulose in the resurrection plant Craterostigma plantagineum

    J. Exp. Bot.

    (2016)
  • D. Osuna

    Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings

    Plant J.

    (2007)
  • M. Kabbage et al.

    The life and death of a plant cell

    Annu. Rev. Plant Biol.

    (2017)
  • D. Nguyen et al.

    Van How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory

    Plant Mol. Biol.

    (2016)
  • N. Suzuki

    Hormone signaling pathways under stress combinations

    Plant Signal. Behav.

    (2016)
  • R. Valluru et al.

    Foliar abscisic acid-to-ethylene accumulation and response regulate shoot growth sensitivity to mild drought in wheat

    Front. Plant Sci.

    (2016)
  • K. Prado

    Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins

    Plant Cell

    (2013)
  • Cited by (15)

    • Optimization of regeneration and Agrobacterium tumefaciens-mediated transient transformation systems for Australian native extremophile, Tripogon loliiformis

      2020, Journal of King Saud University - Science
      Citation Excerpt :

      A unique group of 135 angiosperm species from 13 families, commonly stated as resurrection plants, can tolerate up to 95% water loss (desiccation) in vegetative tissues for prolonged periods without loss of viability (Challabathula and Bartels, 2013; Farrant et al., 2012; Gaff, 1977; Gaff and Oliver, 2013). The plant’s ability to tolerate desiccation is most probably due to a complex assortment of multigenic and multifactorial machinery, for instance, morphological and anatomical changes (Asami et al., 2018; Sherwin and Farrant, 1996, 1998), shutdown of photosynthesis (Aidar et al., 2010; Dinakar et al., 2012), instigation of antioxidant systems (Sherwin and Farrant, 1998), variations in carbohydrate levels (Benina et al., 2013) and cell wall properties (Moore et al., 2009; Vicré et al., 1999). Tripogon loliiformis or five-minute grass belongs to the genus Tripogon, subfamily Chloridoideae and therefore the family Poaceae.

    • Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response

      2019, Journal of Plant Physiology
      Citation Excerpt :

      Stress-induced starch degradation increases carbon flux into the hexose phosphate pool (Fig. 1), and the spectrum of sugars produced from this pool will reflect the species, tissue, and type of stress experienced (Keunen et al., 2013; Krasavina et al., 2014). Different sugars affect physiological processes in distinct ways as shown in Table 1A: 1) Raffinose family oligosaccharides (RFOs) are superior osmolytes and ROS scavengers compared to other sugars (Asami et al., 2018; Keunen et al., 2013); 2) The ratio of hexose to sucrose can influence organ size through their distinct regulation of cell osmotic potential and mitotic activity (Beckles et al., 2012; Ruan, 2014); 3) There are also sugar-specific signaling transduction pathways: for example, the Hexokinase (HXK) and the Target of Rapamycin (TOR) pathways are regulated by glucose, the Trehalose-6-phosphate / Sucrose non-fermenting related kinase (T6P/SnRK) pathway by trehalose, and the hexokinase-autonomous sucrose-specific pathway by sucrose (Baena-Gonzalez et al., 2007; Chiou and Bush, 1998; Martin and Hall, 2005; Martinez-Noel and Tognetti, 2018; Rolland et al., 2006; Wingler, 2018). Clearly, the secondary effect of concentration changes in these respective sugars will be highly context-dependent.

    View all citing articles on Scopus
    View full text