Conserved autophagy and diverse cell wall composition: unifying features of vascular tissues in evolutionarily distinct plants

Abstract

Background and Aims The formation of multifunctional vascular tissues represents a significant advancement in plant evolution. Differentiation of conductive cells is specific, involving two main pathways – protoplast clearance and cell wall modification. In xylogenesis, autophagy is a crucial process of the complete protoplast elimination in tracheary elements, whose cell wall also undergoes strong changes. Knowledge pertaining to living sieve elements, which lose most of their protoplast during phloemogenesis, remains limited. We hypothesized that autophagy plays a critical role, not only in xylem complete cytoplasmic clearance but also in partial degradation in phloem. Cell wall elaborations of mature sieve elements are not so extensive. These analyses performed on evolutionary diverse model species potentially make it possible to understand phloemogenesis to an equal extent as xylogenesis. Methods We investigated the distribution of ATG8 protein, which is an autophagy marker, and cell wall components in the roots of ferns, gymnosperms, and angiosperms (monocots, dicot herbaceous plants, and trees). Furthermore, we conducted a bioinformatic analysis of complete data on ATG8 isoforms for Ceratopteris richardii. Key Results The presence of ATG8 protein was confirmed in both tracheary elements and sieve elements; however, the composition of cell wall components varied considerably among vascular tissues in the selected plants. Arabinogalactan proteins and β-1,4-galactan were detected in the roots of all studied species, suggesting their potential importance in phloem formation or function. In contrast, no evolutionary pattern was observed for xyloglucan, arabinan, or homogalacturonan. Conclusions Our study's findings indicate that the involvement of autophagy in plants is universal during the development of tracheary elements that are dead at maturity and sieve elements that remain alive. Given the conserved nature of autophagy, and its function in protoplast degradation for uninterrupted flow, autophagy may have played a vital role in the development of increasingly complex biological organizations, including the formation of vascular tissues. On the other hand, different cell wall compositions of xylem and phloem in different species may indicate diverse functionality and potential of substance transport, which is critical in plant evolution.