Cell wall modification by the xyloglucan endotransglycoslylase/hydroxylase XTH19 influences Arabidopsis thaliana freezing tolerance after cold and sub-zero acclimation

Authors: TAKAHASHI, DAISUKE - Saitama University; JOHNSON, KIM - La Trobe University; Tuong, Tan; SAMPATHKUMAR, ARUN - Max Planck Institute Of Molecular Plant Physiology; Livingston, David; KOPKA, JOACHIM - Max Planck Institute Of Molecular Plant Physiology; KUROHA, TAKESHI - Tohoku University; YOKOYAMA, RYUSUKE - Tohoku University; NISHITANI, KAZUHIKO - Tohoku University; ZUTHER, ELLEN - Max Planck Institute Of Molecular Plant Physiology; HINCHA, DIRK - Max Planck Institute Of Molecular Plant Physiology

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2020
Publication Date: 2/5/2021
Citation: Takahashi, D., Johnson, K., Tuong, T.D., Sampathkumar, A., Livingston, D.P., Kopka, J., Kuroha, T., Yokoyama, R., Nishitani, K., Zuther, E., Hincha, D. 2021. Cell wall modification by the xyloglucan endotransglycoslylase/hydroxylase XTH19 influences Arabidopsis thaliana freezing tolerance after cold and sub-zero acclimation. Plant Cell and Environment. 44:915-930.

Interpretive Summary: Plants typically become significantly more freezing tolerant after a period of acclimation at below freezing temperatures but before injury occurs. This acclimation usually occurs at a temperature of around -3C for up to 48h and is called subzero acclimation. The mechanism used by plants to increase freezing tolerance during subzero acclimation is largely unknown but modification of cell walls are known to have a an effect on freezing tolerance. In this study, Arabidopsis mutants were used to study various modifications of cell walls. It was discovered that a xyloglucan enzyme that has the ability to confer structural changes in cell walls was significantly changed in mutant plants. These changes were localized to the vascular system using 3D reconstruction and fluorescent microscopy. Understanding specific adaptations used by plants to withstand freezing stresses will help breeders select individual genes for modification to increase freezing tolerance.

Technical Abstract: Freezing is an important environmental stress factor for plants. It triggers the formation of ice crystals in the intercellular spaces of tissues and leads to cell dehydration. The cell wall could play an important role in determining freezing tolerance because its properties will strongly influence cell deformation during freeze-thaw induced dehydration and rehydration. Many plant species increase their freezing tolerance during exposure to low, non-freezing temperatures in a process termed cold acclimation. In addition, exposure to mild freezing temperatures after cold acclimation has been demonstrated to evoke further freezing tolerance and is referred to as sub-zero acclimation. Previous transcriptome and proteome analyses have indicated that cell wall remodeling may be important during sub-zero acclimation. In the present study, we have used a combination of immunohistochemistry, chemical analysis of cell wall composition and infrared spectrometry to characterize the differences in the cell walls of wild type Columbia-0 Arabidopsis plants and plants with a T-DNA insertion in the XTH19 gene, encoding a xyloglucan endotransglucosylase/hydrolase. The mutant showed reduced freezing tolerance both after cold and sub-zero acclimation, which was accompanied by changes in cell wall composition and structure. Most strikingly, immunohistochemistry in combination with 3D reconstruction of hypocotyls indicated that epitopes of the xyloglucan-specific antobody LM25 were specifically abundant in the vasculature of WT plants after sub-zero acclimation, while a mutation in the XTH19 gene resulted in a diffuse localization of the epitopes. Taken together, our data show the importance of cell wall remodeling during low temperature acclimation in Arabidopsis.