Tài liệu Báo cáo khoa học: A systems biology approach for the analysis of carbohydrate dynamics

A systems biology approach for the analysis of

carbohydrate dynamics during acclimation to low

temperature in Arabidopsis thaliana

Thomas Na¨gele, Benjamin A. Kandel*, Sabine Frana*, Meike Meißner and Arnd G. Heyer

Biologisches Institut, Abteilung Pflanzenbiotechnologie, Universita¨t Stuttgart, Germany

Introduction

Low temperature is an important environmental factor

affecting plant growth, and constraining crop produc￾tivity and species distribution [1,2]. Whereas many

tropical and subtropical species have only limited

capacities to cope with low temperature, plants from

temperate climates, such as Arabidopsis thaliana, grow

at low temperature and can increase their freezing tol￾erance when exposed to low but nonfreezing tempera￾tures, in a process termed cold acclimation [3]. The

acclimation process is a very complex phenomenon

comprising numerous changes in metabolism and

affecting gene expression, membrane structure, and the

composition of proteins and primary and secondary

metabolites [4–7]. In this context, many studies have

shown a strong correlation between changes in the

regulation of central carbohydrate metabolism and

freezing tolerance [4,8]. In Arabidopsis, the development

of leaves at low temperature causes reprogramming of

Keywords

acclimation dynamics; Arabidopsis;

carbohydrate metabolism; freezing

tolerance; mathematical modelling

Correspondence

T. Na¨gele, Biologisches Institut, Abteilung

Pflanzenbiotechnologie, Universita¨t

Stuttgart, Pfaffenwaldring 57, D-70550

Stuttgart, Germany

Fax: +49 711 685 65096

Tel: +49 711 685 69141

E-mail: [email protected]

*These authors contributed equally to this

work

(Received 11 August 2010, revised 22 Sep￾tember 2010, accepted 22 November 2010)

doi:10.1111/j.1742-4658.2010.07971.x

Low temperature is an important environmental factor affecting the perfor￾mance and distribution of plants. During the so-called process of cold

acclimation, many plants are able to develop low-temperature tolerance,

associated with the reprogramming of a large part of their metabolism. In

this study, we present a systems biology approach based on mathematical

modelling to determine interactions between the reprogramming of central

carbohydrate metabolism and the development of freezing tolerance in two

accessions of Arabidopsis thaliana. Different regulation strategies were

observed for (a) photosynthesis, (b) soluble carbohydrate metabolism and

(c) enzyme activities of central metabolite interconversions. Metabolism of

the storage compound starch was found to be independent of accession￾specific reprogramming of soluble sugar metabolism in the cold. Mathemati￾cal modelling and simulation of cold-induced metabolic reprogramming

indicated major differences in the rates of interconversion between the

pools of hexoses and sucrose, as well as the rate of assimilate export to

sink organs. A comprehensive overview of interconversion rates is pre￾sented, from which accession-specific regulation strategies during exposure

to low temperature can be derived. We propose this concept as a tool for

predicting metabolic engineering strategies to optimize plant freezing toler￾ance. We confirm that a significant improvement in freezing tolerance in

plants involves multiple regulatory instances in sucrose metabolism, and

provide evidence for a pivotal role of sucrose–hexose interconversion in

increasing the cold acclimation output.

Abbreviations

eInv, extracellular invertase; FrcK, fructokinase; FW, fresh weight; GlcK, glucokinase; LT50, 50% lethality temperature; nInv, neutral

invertase; Rsch, Rschew; SD, standard deviation; SPS, sucrose phosphate synthase; vInv, vacuolar invertase.

506 FEBS Journal 278 (2011) 506–518 ª 2010 The Authors Journal compilation ª 2010 FEBS