Arabidopsis DEFECTIVE KERNEL1 regulates cell wall composition and axial growth in the inflorescence stem

Abstract

Axial growth in plant stems requires a fine balance between elongation and stem mechanical reinforcement to ensure mechanical stability. Strength is provided by the plant cell wall, the deposition of which must be coordinated with cell expansion and elongation to ensure that integrity is maintained during growth. Coordination of these processes is critical and yet poorly understood. The plant‐specific calpain, DEFECTIVE KERNEL 1 ( DEK 1), plays a key role in growth coordination in leaves, yet its role in regulating stem growth has not been addressed. Using plants overexpressing the active CALPAIN domain of DEK 1 ( CALPAIN OE ) and a DEK 1 knockdown line ( ami RNA ‐ DEK 1 ), we undertook morphological, biochemical, biophysical, and microscopic analyses of mature inflorescence stems. We identify a novel role for DEK 1 in the maintenance of cell wall integrity and coordination of growth during inflorescence stem development. CALPAIN OE plants are significantly reduced in stature and have short, thickened stems, while ami RNA ‐ DEK 1 lines have weakened stems that are unable to stand upright. Microscopic analyses of the stems identify changes in cell size, shape and number, and differences in both primary and secondary cell wall thickness and composition. Taken together, our results suggest that DEK 1 influences primary wall growth by indirectly regulating cellulose and pectin deposition. In addition, we observe changes in secondary cell walls that may compensate for altered primary cell wall composition. We propose that DEK 1 activity is required for the coordination of stem strengthening with elongation during axial growth.

Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy

“…When a stem of a mature plant is analyzed with laser beams overlapped over an area of 200–300 μm in diameter, the regions or tissues with the highest cellulose content would dominate SFG spectral features. ,,− , In stems, cell walls of the interfascicular fiber (providing mechanical supports) and xylem (transporting water) tissues are much thicker and have much higher cellulose contents than those of other tissues. , If the focus of study is to find correlations between cell wall structures of these dominant tissues and the overall cellulose contents, the area-averaged analysis might be acceptable since errors due to minor tissues with much less cellulose contents would be small. However, such studies could not unveil structures of other tissues with different biological functions, such as the phloem cells translocating products of photosynthesis (i.e., carbohydrates), the cortex region containing the chloroplast and also storing carbohydrates or other substances, and the epidermis providing mechanical strength and protecting the stem from external stimuli .…”

“…However, such studies could not unveil structures of other tissues with different biological functions, such as the phloem cells translocating products of photosynthesis (i.e., carbohydrates), the cortex region containing the chloroplast and also storing carbohydrates or other substances, and the epidermis providing mechanical strength and protecting the stem from external stimuli . If specific tissues that are present as a minor component in volume fraction play dominant roles in the physical properties of the entire stem, then the volume-averaged information may not be able to fully explain the measured physical properties. , The BB-SFG microscope system allows one to obtain tissue-specific SFG spectral information.…”

With an Ear Up against the Wall: An Update on Mechanoperception in Arabidopsis

“…Indeed, the membrane-localized DEK1 protein undergoes autolytic cleavage and the calpain domain is released into the cytosol [ 158 ]. While DEK1 activity is associated with epidermal cell differentiation [ 159 , 160 ], embryo development [ 161 ], and cell division patterns [ 162 ], DEK1 activity also affects cell wall composition by primarily affecting cellulose and pectin deposition [ 163 ]. Surprisingly, the calpain domain itself is sufficient to complement dek1 mutants [ 158 ].…”

The pillars of land plants: new insights into stem development

“…The highly conserved DEK1 Ca++-dependent calpain has been implicated as a component of this mechanosensing mechanism [ 51 •• ]. Reflecting the importance of DEK1 in regulating cell wall properties, DEK1 knockdown reduced deposition of cellulose and pectin, resulting in weak stems [ 52 ].…”