The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation    

Abstract

Trehalose 6-P (T6P) is a sugar signal in plants that inhibits SNF1-related protein kinase, SnRK1, thereby altering gene expression and promoting growth processes. This provides a model for the regulation of growth by sugar. However, it is not known how this model operates under sink-limited conditions when tissue sugar content is uncoupled from growth. To test the physiological importance of this model, T6P, SnRK1 activities, sugars, gene expression, and growth were measured in Arabidopsis (Arabidopsis thaliana) seedlings after transfer to cold or zero nitrogen compared with sugar feeding under optimal conditions. Maximum in vitro activities of SnRK1 changed little, but T6P accumulated up to 55-fold, correlating with tissue Suc content in all treatments. SnRK1-induced and -repressed marker gene expression strongly related to T6P above and below a threshold of 0.3 to 0.5 nmol T6P g 21 fresh weight close to the dissociation constant (4 mM) of the T6P/ SnRK1 complex. This occurred irrespective of the growth response to Suc. This implies that T6P is not a growth signal per se, but through SnRK1, T6P primes gene expression for growth in response to Suc accumulation under sink-limited conditions. To test this hypothesis, plants with genetically decreased T6P content and SnRK1 overexpression were transferred from cold to warm to analyze the role of T6P/SnRK1 in relief of growth restriction. Compared with the wild type, these plants were impaired in immediate growth recovery. It is concluded that the T6P/SnRK1 signaling pathway responds to Suc induced by sink restriction that enables growth recovery following relief of limitations such as low temperature.

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

“…In one scenario, KIN10-mediated energy signaling regulates hypocotyl elongation by acting upon phytohormone signaling, potentially through PIFs (Lilley et al, 2012). In a different and nonexclusive scenario, SnRK1-mediated alterations in metabolic enzyme activity and growth-related transcripts prime the hypocotyls to capitalize upon increased Suc availability (Nunes et al, 2013a). This is an interesting question in the case of hypocotyl elongation, which arises from cell expansion rather than growth through cell division and biomass accumulation per se (Gendreau et al, 1997).…”

“…Growth is increased by Suc in the presence of Tre6P (Schluepmann et al, 2003;Paul et al, 2010), but the lack of a quantitative (correlative) relationship between relative growth rates and [Tre6P] suggests that a threshold [Tre6P] is required for growth to occur (Nunes et al, 2013a(Nunes et al, , 2013b. Therefore, it has been suggested that control of KIN10/11 by [Tre6P] may prime the regulation of growth-related genes to capitalize upon increased energy availability, rather than by inducing growth directly (Nunes et al, 2013a(Nunes et al, , 2013b. Remarkably, the impact of this pathway is sufficiently global that its manipulation can increase maize (Zea mays) yields by almost 50% (Nuccio et al, 2015) and increase the yield and drought tolerance of wheat (Triticum aestivum; Griffiths et al, 2016).…”

“…Signaling by Tre6P and KIN10 is also important for the regulation of growth rates. Growth is increased by Suc in the presence of Tre6P (Schluepmann et al, 2003;Paul et al, 2010), but the lack of a quantitative (correlative) relationship between relative growth rates and [Tre6P] suggests that a threshold [Tre6P] is required for growth to occur (Nunes et al, 2013a(Nunes et al, , 2013b. Therefore, it has been suggested that control of KIN10/11 by [Tre6P] may prime the regulation of growth-related genes to capitalize upon increased energy availability, rather than by inducing growth directly (Nunes et al, 2013a(Nunes et al, , 2013b.…”

“…Both SnRK1-and hexokinasemediated sugar signaling involve specific sugars functioning as signaling molecules that provide cellular information concerning sugar availability. For example, SnRK1 activity is thought to be regulated by trehalose-6-P (Tre6P), whose concentration tracks the cellular concentration of Suc (Lunn et al, 2006;Zhang et al, 2009;Nunes et al, 2013aNunes et al, , 2013bYadav et al, 2014). Tre6P is synthesized from UDP Glc and Glc-6-P, which are derived from mobilized and transported Suc, and also directly from photosynthesis.…”

“…Of 11 TPS homologs encoded by the Arabidopsis genome, TREHALOSE-6-PHOSPHATE SYNTHASE1 (TPS1) synthesizes Tre6P in plants (Gómez et al, 2010;Vandesteene et al, 2010), and TPS2 and TPS4 are catalytically active in yeast complementation assays (Delorge et al, 2015). Tre6P is believed to regulate SnRK1-mediated signaling by suppressing the activity of SNF1-RELATED PRO-TEIN KINASE1.1 (KIN10/AKIN10/SnRK1.1), which is a catalytic subunit of SnRK1 that is fundamental to the signaling role of SnRK1 (Baena-González et al, 2007;Zhang et al, 2009;Nunes et al, 2013aNunes et al, , 2013b.…”