Cold stress and freezing tolerance negatively affect the fitness of Arabidopsis thaliana accessions under field and controlled conditions

Maximilian Boinot,Majken Pagter,Ellen Zuther,Karin Koehl,Esra Karakas

doi:10.1007/s00425-021-03809-8

Maximilian Boinot, Majken Pagter + Show 3 more

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https://doi.org/10.1007/s00425-021-03809-8

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Abstract

Main conclusionHigher acclimated freezing tolerance improved winter survival, but reduced reproductive fitness of Arabidopsis thaliana accessions under field and controlled conditions.Low temperature is one of the most important abiotic factors influencing plant fitness and geographical distribution. In addition, cold stress is known to influence crop yield and is therefore of great economic importance. Increased freezing tolerance can be acquired by the process of cold acclimation, but this may be associated with a fitness cost. To assess the influence of cold stress on the fitness of plants, long-term field trials over 5 years were performed with six natural accessions of Arabidopsis thaliana ranging from very tolerant to very sensitive to freezing. Fitness parameters, as seed yield and 1000 seed mass, were measured and correlation analyses with temperature and freezing tolerance data performed. The results were compared with fitness parameters from controlled chamber experiments over 3 years with application of cold priming and triggering conditions. Winter survival and seed yield per plant were positively correlated with temperature in field experiments. In addition, winter survival and 1000 seed mass were correlated with the cold-acclimated freezing tolerance of the selected Arabidopsis accessions. The results provide strong evidence for a trade-off between higher freezing tolerance and reproductive fitness in A. thaliana, which might have ecological impacts in the context of global warming.

Highlights

Temperature is among the most important abiotic factors that influence the geographical distribution, growth and fitness of plants
The aim of this study was to assess the influence of cold temperature, especially of recurring cold stress events, on fitness parameters of natural accessions of Arabidopsis thaliana, ranging from very low to very high natural freezing tolerance
On the Arabidopsis accessions are divided in winter and summer annuals, but transitions between these types are known depending on the temperature conditions (Wilczek et al 2009) and under the here described conditions all accessions performed as winter annuals

Summary

Introduction

Temperature is among the most important abiotic factors that influence the geographical distribution, growth and fitness of plants. High as well as low temperatures decrease the yield of annual crops (Yadav 2010; Sanghera et al 2011; Powell et al 2012) and delimit their natural occurrence (Kreyling et al 2015). Plants have evolved mechanisms to cope with cold stress. In late autumn and the beginning of winter, when air temperatures decrease, plants increase their freezing tolerance after exposure to low, but non-freezing temperatures in a seasonal process called cold acclimation (Levitt 1980). Comprehensive energy-demanding and potentially costly metabolic and transcriptomic reprogramming accompanies this acclimation (Cook et al 2004; Hannah et al 2005; Maruyama et al 2009; Hincha et al 2012), which is partly driven by the CBF

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