Xylem is the main route for transporting water, minerals and a myriad of signalling molecules within the plant. With its onset during early embryogenesis, the development of the xylem relies on hormone gradients, the activity of unique transcription factors, the distribution of mobile microRNAs, and receptor-ligand pathways.These regulatory mechanisms are often interconnected and together contribute to the plasticity of this water-conducting tissue. Environmental stresses, such as drought and salinity, have a great impact on xylem patterning. A better understanding of how the structural properties of the xylem are regulated in normal and stress conditions will be instrumental in developing crops of the future. In addition, vascular wilt pathogens that attack the xylem are becoming increasingly problematic.Further knowledge of xylem development in response to these pathogens will bring new solutions against these diseases. In this review, we summarize recent findings on the molecular mechanisms of xylem formation that largely come from Arabidopsis research with additional insights from tomato and monocot species. We emphasize the impact of abiotic factors and pathogens on xylem plasticity and the urgent need to uncover the underlying mechanisms. Finally, we discuss the multidisciplinary approach to model xylem capacities in crops. K E Y W O R D S abiotic stresses, eudicots and monocots, phenotypic and modelling, wilt pathogens, xylem development 1 | INTRODUCTION Water is arguably the most important component of life. Vascular plants transport water and dissolved nutrients efficiently from the roots to all above-ground parts using a specialized tissue called the xylem. This tissue is composed of lignified conducting elements, fibres, and parenchyma cells. The process of xylem development is fascinating and has attracted developmental biologists for more than a century. The early studies on xylem formation demonstrated wounding-induced xylogenesis as well as the formation of xylem from callus and transdifferentiation of the tissue culture cells into the xylem cells (Fukuda &

Plant meristems require a constant supply of photoassimilates and hormones to the dividing meristematic cells. In the growing root, such supply is delivered by protophloem sieve elements. Due to its preeminent function for the root apical meristem, protophloem is the first tissue to differentiate. This process is regulated by a genetic circuit involving in one side the positive regulators DOF transcription factors, OCTOPUS (OPS) and BREVIX RADIX (BRX), and in the other side the negative regulators CLAVATA3/EMBRYO SURROUNDING REGION RELATED (CLE) peptides and their cognate receptors BARELY ANY MERISTEM (BAM) receptor-like kinases. brx and ops mutants harbor a discontinuous protophloem that can be fully rescued by mutation in BAM3, but is only partially rescued when all three known phloem-specific CLE genes, CLE25/26/45 are simultaneously mutated. Here we identify a CLE gene closely related to CLE45, named CLE33. We show that double mutant cle33cle45 fully suppresses brx and ops protophloem phenotype. CLE33 orthologs are found in basal angiosperms, monocots, and eudicots, and the gene duplication which gave rise to CLE45 in Arabidopsis and other Brassicaceae appears to be a recent event. We thus discovered previously unidentified Arabidopsis CLE gene that is an essential player in protophloem formation.

Xylem is a main road in plant long-distance communication. Through xylem plants transport water, minerals and myriad of signaling molecules. With the onset during early embryogenesis, the development of xylem tissues relays on hormone gradients, activity of unique transcription factors, distribution of mobile miRNAs and receptor-ligand pathways. These regulatory mechanisms are often interconnected and all together contribute to the plasticity of water conducting tissue. Remarkably, root xylem carries water to all above-ground organs and therefore influences all aspects of plant growth. Because of the global warming and increasing water deficit, we need to come up with solutions for the crops of the future. It is clear that structure of water conducting elements directly impacts water transport within the plant. Among plant pathogens- vascular wilts attacking xylem -are the most harmful. Our knowledge about xylem anatomy and rewiring ability could bring the solutions against these diseases. In this review we summarize the recent findings on the molecular mechanisms of xylem formation with a special attention to the cellular changes, and cell wall rearrangements that are necessary to create functional capillaries. We emphasize the impact of abiotic factors and pathogens on xylem plasticity and discuss multidisciplinary approach to model xylem in crops.

Plant meristems require a constant supply of photoassimilates and hormones to the dividing meristematic cells. In the growing root, such supply is delivered by protophloem sieve elements (1). Due to its preeminent function for the root apical meristem, protophloem is the first tissue to differentiate. This process is regulated by a genetic circuit involving in one-side the positive regulators DOF transcription factors (2, 3), OCTOPUS (OPS)(4) and BREVIX RADIX (BRX)(5), and in the other-side the negative regulators CLAVATA3/EMBRYO SURROUNDING REGION RELATED (CLE) peptides and their cognate receptors BARELY ANY MERISTEM (BAM) receptor-like kinases and co-receptors CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIKs)(2, 6-8). brx and ops mutants harbor a discontinuous protophloem (4, 5) that can be fully rescued by mutation in BAM3 (5) but only partially rescued by multiple mutations in all three known phloem-specific CLE genes, CLE25/26/45 (2, 6). These observations suggest that one or more additional CLE peptides play a role in protophloem formation. By reanalyzing Arabidopsis genome, we have identified a novel CLE gene closely related to CLE45, named CLE33, that is expressed in developing protophloem and is perceived by BAM3. Mutations in CLE33 and CLE45 are together sufficient to fully suppress brx and ops discontinuous protophloem phenotype. Furthermore, in these mutants we observed ectopic protophloem differentiation in neighboring cells, supporting the current model where phloem-specific CLE peptides act as paracrine signals to maintain a single functional protophloem cell file (2). CLE33 orthologs are found in basal angiosperms, monocots and eudicots, and the gene duplication giving rise to CLE45 in Arabidopsis and other Brassicaceae appears to be a recent event. We, thus, have discovered a novel peptide gene that is an ancient angiosperms’ CLE gene, and an essential player in the genetic circuit controlling protophloem formation.

Xylem is a main road in plant long-distance communication. Through xylem plants transport water, minerals and myriad of signaling molecules. With the onset during early embryogenesis, the development of xylem tissues relays on hormone gradients, activity of unique transcription factors, distribution of mobile miRNAs and receptor-ligand pathways. These regulatory mechanisms are often interconnected and all together contribute to the plasticity of water conducting tissue. Remarkably, root xylem carries water to all above-ground organs and therefore influences all aspects of plant growth. Because of the global warming and increasing water deficit, we need to come up with solutions for the crops of the future. It is clear that structure of water conducting elements directly impacts water transport within the plant. Among plant pathogens- vascular wilts attacking xylem -are the most harmful. Our knowledge about xylem anatomy and rewiring ability could bring the solutions against these diseases. In this review we summarize the recent findings on the molecular mechanisms of xylem formation with a special attention to the cellular changes, and cell wall rearrangements that are necessary to create functional capillaries. We emphasize the impact of abiotic factors and pathogens on xylem plasticity and discuss multidisciplinary approach to model xylem in crops.