Overexpression of Arabidopsis Hexokinase in Tomato Plants Inhibits Growth, Reduces Photosynthesis, and Induces Rapid Senescence

Abstract

Sugars are key regulatory molecules that affect diverse processes in higher plants. Hexokinase is the first enzyme in hexose metabolism and may be a sugar sensor that mediates sugar regulation. We present evidence that hexokinase is involved in sensing endogenous levels of sugars in photosynthetic tissues and that it participates in the regulation of senescence, photosynthesis, and growth in seedlings as well as in mature plants. Transgenic tomato plants overexpressing the Arabidopsis hexokinase-encoding gene AtHXK1 were produced. Independent transgenic plants carrying single copies of AtHXK1 were characterized by growth inhibition, the degree of which was found to correlate directly to the expression and activity of AtHXK1. Reciprocal grafting experiments suggested that the inhibitory effect occurred when AtHXK1 was expressed in photosynthetic tissues. Accordingly, plants with increased AtHXK1 activity had reduced chlorophyll content in their leaves, reduced photosynthesis rates, and reduced photochemical quantum efficiency of photosystem II reaction centers compared with plants without increased AtHXK1 activity. In addition, the transgenic plants underwent rapid senescence, suggesting that hexokinase is also involved in senescence regulation. Fruit weight, starch content in young fruits, and total soluble solids in mature fruits were also reduced in the transgenic plants. The results indicate that endogenous hexokinase activity is not rate limiting for growth; rather, they support the role of hexokinase as a regulatory enzyme in photosynthetic tissues, in which it regulates photosynthesis, growth, and senescence.

Quantitative metabolic profiling by 1-dimensional 1H-NMR analyses: application to plant genetics and functional genomics

“…These data, which clearly differ from those obtained with fruit and leaves (Menu et al 2003;Roessner-Tunali et al 2003), mean that hexokinase over expression does not change the metabolic status of the roots to a significant extent. This confirms conclusions drawn by previous authors (Dai et al 1999) indicating that the general phenotype of HK4 plants was mainly due to hexokinase overexpression in shoots rather than in roots. It may be noted that fumarate contents were clearly increased in HK4 roots compared to WT roots.…”

“…Transformation of plants with hexokinase genes has been conducted as a strategy for studying glucose sensing. Thus, several lines of tomato plants overexpressing Arabidopsis hexokinase 1 (HK4, HK37, HK38) and exhibiting high hexokinase activity in correlation with drastic phenotypic modifications (Dai et al 1999) were produced. Recently, comprehensive metabolic profiling studies on leaves and fruits of these transformant lines were conducted using GC-MS, conventional spectrophotometric and liquid chromatographic methodologies (Menu et al 2003;Roessner-Tunali et al 2003).…”

“…AtHK1 hexokinase transformants [HK4, (Dai et al 1999)] and wild type (WT) tomato (Lycopersicon esculentum L. strain MP-1) plants were cultivated in controlled hydroponic conditions (Baldet et al 2002). Eight WT plants and 16 transformant plants were used for each culture.…”

Mathematical modeling reveals that metabolic feedback regulation of SnRK1 and hexokinase is sufficient to control sugar homeostasis from energy depletion to full recovery

“…In this context, previous studies reporting on AtHXK1 overexpression in tomato and Arabidopsis found a decreased expression of photosynthetic genes and an inhibition of growth (Dai et al, 1999; Kelly et al, 2012). This physiological output is similar to the output being characteristic for SnRK1 activity (Baena-Gonzalez et al, 2007), and hence it supports a model of Hxk/T6P/SnRK1-interdependent signaling.…”

The changes of organelle ultrastructure and Ca2+ homeostasis in maize mesophyll cells during the process of drought-induced leaf senescence

“…Although senescence occurs in an age-dependant manner in many species (Noode'n, 1988), its initiation and progression can be modulated by a variety of environmental factors such as temperature, mineral deficiency, and drought conditions, as well as by internal factors such as plant growth regulators (Grbić and Bleecker, 1995;Nam, 1997;Weaver et al 1997;Dai et al 1999). It has proved that drought, darkness, leaf detachment, and the hormones abscisic acid (ABA) and ethylene induce leaf yellowing, which is an good indicator of leaf senescence, whereas, to different extent.…”