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\begin{document}

\title{Understanding the Root Xylem Plasticity for Designing Resilient Crops}



\author[1]{Salves Cornelis}%
\author[1]{Ora  Hazak}%
\affil[1]{University of Fribourg}%


\vspace{-1em}



  
  \date{May 08, 2024}


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\selectlanguage{english}
\begin{abstract}
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.%
\end{abstract}%



\sloppy


Review for the Special Issue of Plant, Cell and Environment ``Root
Phenotypes for the Future''

\textbf{Understanding the Root Xylem Plasticity for Designing Resilient
Crops}

\textbf{}Salves Cornelis\textsuperscript{1} and Ora
Hazak\textsuperscript{1*}

Department of Biology, University of Fribourg, Chemin du Musee 10, 1700
Fribourg, Switzerland

*- Corresponding author ora.hazak@unifr.ch

\textbf{Abstract} 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.

\textbf{Highlights}

\begin{itemize}
\tightlist
\item
  Making xylem vessels: differentiation of xylem cells happens gradually
  from the precursors to fully functional hollow lignified capillaries
\item
  Molecular genetic framework of xylem formation: from hormones and
  transcription factors to small regulatory RNAs and peptide-receptor
  pathways
\item
  Abiotic stresses influence xylem patterning
\item
  To fight xylem pathogens, plants produce polymers that block the
  infection and create new xylem elements to overcome the contaminated
  vessels
\item
  The multidisciplinary approach to model the plant water use in
  different plant species and crop varieties will help in designing
  resilient crops
\end{itemize}

Water is arguably the most important component for life. Land plants
efficiently transport water and dissolved nutrients from the roots to
all above ground parts using specialized tissue called xylem composed of
lignified conducting elements, fibers and parenchyma cells.

The process of xylem development is fascinating and has been attracting
developmental biologists for more than a century. The early studies on
xylem formation demonstrated wounding-induced xylogenesis as well as
formation of xylem from callus and trans-differentiation of the cell
tissue culture cells into the xylem cells (V\selectlanguage{ngerman}öchting 1892, Simon 1908,
Jacobs 1952, Wetmore and Rier 1963, Fukuda and Komamine 1980). In this
review we summarize the recent advances in root xylem development
research with a special attention to environmental inputs that
contribute to the patterning of this tissue. Our goal is to highlight
the importance of xylem research in the light of global warming and
increasing risk of vascular wilt diseases. First, we introduce the
developmental steps that xylem initials undergo to become functional
conducting elements. Later we discuss the molecular mechanisms and the
key players in formation of this tissue. Afterwards, we focus on the
abiotic stresses that modify xylem and vascular wilt pathogens and the
ways plants fight against them. Finally, we summarize and discuss a
multidisciplinary approach to phenotype and model xylem capacity.

\textbf{1. Making xylem vessels: from xylem precursors to fully
functional capillaries}

Development of xylem tissue can be divided into early steps, when the
totipotent cells commit to create xylem, and to later steps- when the
xylem precursors transform to functional capillaries. Because the fully
differentiated xylem cells are not alive, the developmental plasticity
can be rather observed in the early steps. However, after the cell
clearing, the surrounding procambium and later parenchyma cells
contribute to plasticity when non-cell autonomously acting in final
steps in xylem maturation (Bollhöner, Zhang et al. 2013, Pesquet, Zhang
et al. 2013) and in case of pathogen infection- with secreting polymers
to block the propagation (reviewed in (Yadeta and Thomma 2013, Kashyap,
Planas-Marques et al. 2021).

In Arabidopsis the first provascular cells originate in the early
embryogenesis, when at the 16-cell stage the inner lower cells divide
periclinally to give rise to the ground and vascular tissue initials
(Scheres, Wolkenfelt et al. 1994) (Figure 1A). Later on, the provascular
initials through formative divisions create initials for pericycle and
procambium. Remarkably, while the pericycle initials will only divide
anticlinally from now on, the procambium initials will continue
periclinal divisions giving rise to the future xylem, phloem and
procambium tissues. At the early globular stage, the most apical
suspensor cell becomes a hypophysis that will later divide
asymmetrically giving rise to QC (quiescent center) and columella stem
cell. In the fully mature embryo, the quiescent center (QC) is
surrounded by the stem cells giving rise to all types of root tissues:
initials for the vasculature, the ground tissues, the epidermis and the
lateral root cap and columella. These early developmental steps in
embryogenesis require auxin accumulation towards the apical cell first,
later towards the hypophysis (Friml, Vieten et al. 2003).

Upon seed germination, the embryonic root meristem rapidly produces new
tissues, the root tip emerges and rapidly elongates. Within hours root
tissues undergo differentiation, including functional root hairs and
xylem capillaries to provide with the uptake of water and minerals
(Figure 1B). In the growing primary root, as well as in the growing
lateral root, developing leaf and flower the only primary xylem is
found; this early conducting tissue will be functionally replaced by
metaxylem and later secondary xylem.

In Arabidopsis primary root, the xylem pole is located in the center of
the vascular cylinder and consists of two outermost protoxylem (PX) cell
files and three metaxylem cell files: one inner metaxylem (IMX) and two
outer metaxylem (OMX) cell files (Figure 1B, Figure 2A, D).
Interestingly, that from the very beginning protoxylem and metaxylem
initials have distinct gene expression profiles (Kubo, Udagawa et al.
2005) even though they undergo similar cellular changes and have very
similar function in transporting water. In Tomato primary root (M-82)
the organization of the primary xylem tissue is similar, including two
protoxylem cell files on each side of the xylem pole and double amount
of the metaxylem cell files (six instead of three) (Figure 1B). Not only
on the morphological level, but also on the molecular level xylem
development regulators seem to be conserved between Arabidopsis and
Tomato (Kajala, Gouran et al. 2021). Later in the development of
dicotyledon plant, primary growth will be replaced with secondary growth
and cambium will give rise to all secondary vascular tissues.

Remarkably, xylem differentiation happens gradually- first, the
outermost protoxylem cell files show thickening of the cell wall and
lignification, later on the outermost metaxylem develops thick cell wall
and lignin (Figure 1B), whereas the central metaxylem gets lignified and
fully functional much later.

On the cellular level, protoxylem and metaxylem undergo similar
processes: starting with multiple anticlinal divisions of the xylem
precursor, then elongation, thickening of the cell wall, accumulating
lytic enzymes in the vacuole, secreting lignin monomers to the apoplast
(Schuetz, Benske et al. 2014) and lignification, that will continue
after the cell death (Pesquet, Zhang et al. 2013) (Figure 2B).

The nature of helical pattern the protoxylem cell wall thickening and
later lignification versus metaxylem cell wall thickening and
lignification is not yet fully clear. What are the molecular
determinants that define the pattern of the thickening in the cell wall?
How are they recruited there? The work on LACCASE4/17 elegantly
demonstrated that these enzymes localize to the secondary cell walls of
the developing protoxylem and metaxylem cells (Schuetz, Benske et al.
2014), but what brings them exactly to the sites where the lignin
biosynthesis should take place? Similar to lignification of the
Casparian strips, there might be CASP-like proteins that recruit the
components of this machinery to establish domains of future secondary
cell wall formation (Roppolo, De Rybel et al. 2011, Roppolo and Geldner
2012). Interestingly, in the metaxylem patterning Rho GTPAses have been
demonstrated to play a key role in establishing specific membrane
domains where the microtubules assembly is inhibited (Oda and Fukuda
2013). The same research group later nicely showed that the size of
piths is regulated in a quantitative manner by microtubule- binding
proteins CORD1 and CORD2 (Sasaki, Fukuda et al. 2017). Another question
is how the diameter and the length of the xylem capillaries are
controlled? Answering these questions could help to modify xylem
networks in crops to adapt better to environmental conditions.

Remarkably, while the primary xylem is playing a key role in the water
uptake in the root tips, the major part of the xylem tissues in plants
originate from cambium during secondary growth (De Rybel, Mähönen et al.
2016). Recent advances in our understanding of secondary growth allowed
to trace the origin of cambium. The team led by Mahonnen used an elegant
approach of lineage tracing and molecular genetic studies to show that
xylem-adjacent procambium cell gives rise to the cambium tissue
(Smetana, Mäkilä et al. 2019).

Understanding the secondary xylem developmental switches and better
phenotyping of this tissue will contribute to the further advances in
optimizing xylem networks.

\textbf{2. The molecular genetic framework of xylem formation}

The process of xylem formation can be divided into three steps: first,
the commitment of the totipotent cell to become a precursor of vascular
tissue and later xylem tissue (can be observed in embryo development or
trans-differentiation of xylem parenchyma or mesophyll or callus cells);
second, the differentiation of xylem precursor into conducting element
with the last step of clearing the cytoplasm and organelles; third,
so-called post-mortem differentiation, when the adjacent cells
contribute to the last steps of formation conducting element. Here we
briefly discuss the key players in every step.

\textbf{2.1 Pre-patterning}

The early studies on xylem formation showed that auxin and cytokinin
play a central role in differentiation of this tissue (Jacobs 1952).
With establishing of Arabidopsis as a plant model, the molecular
research on vascular development has been significantly advanced. The
large genetic screens in Arabidopsis could identify additional
components including cytokinin signaling, transcription factors and
micro RNAs that control xylem development (Benfey, Linstead et al. 1993,
Turner and Somerville 1997, Cano-Delgado, Metzlaff et al. 2000, Yokoyama
and Nishitani 2006). Developing molecular tools allowing to visualize
the distribution of the hormone signaling in addition to mutant approach
could demonstrate that auxin is the first signal required for xylem
initiation and differentiation (Ulmasov, Murfett et al. 1997, Friml,
Vieten et al. 2003, Weijers, Schlereth et al. 2006, Herud-Sikimi\selectlanguage{polish}ć, \selectlanguage{english}Stiel
et al. 2021). The molecular mechanism of auxin- induced xylem formation
has been studied in details. The auxin-dependent transcription factor
MONOPTERUS (MP) expressed in embryo, targets TMO5 and TMO7 (TARGET OF
MONOPTERUS 5 and 7)(Schlereth, M\selectlanguage{ngerman}öller et al. 2010), two bHLH
transcription factors. TMO5 creates a complex with LHW (LONESOME
HIGHWAY)- another bHLH transcription factor (Katayama, Iwamoto et al.
2015, Ohashi-Ito, Iwamoto et al. 2019)- to upregulate the expression of
cytokinin biosynthetic enzymes genes LONELY GUY3 and 4 (LOG3 and 4) and
a cytokinin signaling inhibitor ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER
PROTEIN6 (AHP6) in protoxylem cells (Mähönen, Bishopp et al. 2006). The
increase in cytokinin signaling due to up-regulation of LOG3 and LOG4
promotes provascular cell divisions. Interestingly, the overexpression
of TMO5/LHW led to the ectopic xylem vessel differentiation (Katayama,
Iwamoto et al. 2015). In conclusion, the complexes of TMO5/LHW are key
players in production of vascular initial cells.

In addition to MP-mediated pathway, auxin promotes the expression of
Homeodomain-Leucin Zipper III (HD-ZIP III) transcription factors, that
will specify the protoxylem versus metaxylem in a dosage-dependent
manner (Carlsbecker, Lee et al. 2010, Ohashi-Ito, Matsukawa et al.
2013). On the one side, these transcription factors are induced by auxin
and on the other side, they are downregulated by miRNA165/166 diffusing
into the vascular cylinder from endodermis (Carlsbecker, Lee et al.
2010) (Figure 2D). More recently, it has been nicely demonstrated, that
the receptor-like kinases BARELY ANY MERISTEM (BAM1and BAM2) control the
movement of these small regulatory RNAs toward the vasculature and
therefore regulate xylem development. Indeed, in the
\emph{bam1bam2}double mutant the levels of miRNA165/166 in the stele are
reduced, while the expression of HD-ZIP III transcription factors is
increased. These mutants show irregular xylem development: the metaxylem
files develop instead of protoxylem files (Fan, Aguilar et al. 2021).
BAM1 and BAM2 are receptor like kinases that bind small signaling
peptides from CLE (\textbf{CL}AVATA3-\textbf{E}MBRYO-surrounding
region-related) family. It is still not fully clear, if the role of BAMs
in movement of small RNAs depends on the peptide-activation mechanism or
not. Interestingly, the first receptor-like kinases shown to play a role
in embryo radial pattern formation (including provascular tissue
formation) were RPK1(TOAD1) and RPK2(TOAD2) (Nodine, Yadegari et al.
2007). These two receptor-like kinases are expressed in the early
globular embryo and contribute to periclinal cell divisions forming
radial pattern. Later study demonstrated that these receptors are
implicated in CLE peptide perception and in addition to their role in
embryo, are essential in root apical meristem maintenance (Racolta,
Nodine et al. 2018). In conclusion, in addition to the key hormones
establishing vascular tissues, downstream transcription factors,
regulatory RNAs and receptor-like-kinases dependent pathways contribute
to the vascular patterning.

\textbf{2.2 Executors}

Following early specification, xylem initials undergo differentiation
including series of anticlinal divisions, elongation, cell wall
thickening, accumulation of the lytic enzymes and monolignons in the
vacuole, lignification in the secondary cell wall and vacuole disruption
that will end in the cell death (Figure 2B). To initiate this
differentiation program, VASCULAR-RELATED NAC-DOMAIN (VND) 6 and 7
transcription factors act in metaxylem and protoxylem respectively
(Kubo, Udagawa et al. 2005) to induce transcription factors that
activate genes related to secondary cell wall formation and cell death.
To comprehensively characterize the transcriptional regulation of the
enzymes acting in secondary cell wall formation, the regulatory network
has been established (Taylor-Teeples, Lin et al. 2015). Here, using a
combination of gene expression data, the authors isolated 467 xylem
transcription factors that have been used in a yeast-one-hybrid
experiments with promoters of secondary cell wall genes. Interestingly,
this regulatory network identified an upstream regulator of VNDs, could
confirm the known transcription factors like MYB46, and hundreds of
novel regulators (Taylor-Teeples, Lin et al. 2015). The multiple
transcription factors act redundantly to initiate cell wall thickening,
lignification and cell death (Figure 2C). It has been shown, that the
enzyme METACASPASE9 (AtMC9) acts in the degradation of the cell content
after the bursting of the central vacuole leading to the cell death
(Bollhöner, Zhang et al. 2013). Remarkably, the switch to the last step
in xylem differentiation might be strictly controlled by the
environment, because, on the one hand, postponing the death can provide
with more plasticity; on the other hand, it will delay the functionality
of the tissue.

\textbf{3. Effects of abiotic stresses on xylem patterning}

Plants sense the environment and adjust the physiological response to
survive. Among abiotic conditions that impact plant growth are water
availability, light, temperature, soil salinity, nutrients abundance,
soil pH. Remarkably, the molecular mechanisms of sensing the environment
and adaptations have developed on the timeframe of more than 450 million
years, since first plants colonized the land. The key hormone mediating
abiotic stress responses is abscisic acid (ABA), that was already
produced in the algae species, but became a key stress signal only in
the common ancestor of the land plants that developed an ABA-dependent
modulation of PYRABACTIN RESISTANCE 1-like (PYL) protein (Sun, Harpazi
et al. 2019). Here we discuss the effects of abiotic stresses on the
xylem patterning described in the literature. Our better understanding
of how plants react and modify their xylem to drought, salt, or
temperatures will help to better understand how to exploit these traits
and develop resilient crops in the future.

\textbf{3.1 Drought}

The molecular mechanisms of the drought stress have been extensively
studied in the last decades (reviewed in (Yu, Wu et al. 2015,
Martignago, Rico-Medina et al. 2019, Ramachandran, Augstein et al.
2020)). Recent studies could nicely pinpoint a mechanism of ABA-mediated
response to water deficit that involves developmental switch in xylem
cell identity ((Ramachandran, Wang et al. 2018, Bloch, Puli et al.
2019)). Interestingly, that under drought conditions or following ABA
treatment the outer metaxylem cells develop into protoxylem cells with
helical pattern of the secondary cell walls. Morphological changes in
xylem are already visible after a four-hour treatment, and are
reversible showcasing the plasticity of the xylem tissue (Ramachandran,
Augstein et al. 2021). In the most recent study Ramachandran et al show
that differentiation measured by lignification onset of the inner
metaxylem is enhanced by drought and direct application of ABA
(Ramachandran, Augstein et al. 2021). Simultaneously, the fate of the
outer metaxylem is transformed into that of protoxylem (Figure 3).
Conforming with these results, disturbing ABA biosynthesis or its
perception either through application of biosynthesis inhibitor
fluridone, biosynthesis mutants \emph{aba2-1} and \emph{aba3-1,} or the
quadruple ABA receptor mutant \emph{pyr1pyl1pyl2pyl4} show disturbed
xylem or were unable to replicate the drought phenotype (Ramachandran
2018, Bloch 2019). This morphological response to ABA could be explained
as protoxylem cells are less vulnerable to embolism compared to
metaxylem and also may have increased lateral water movement for
embolism repair. The study conducted in maize could show this tendency
(Hwang, Ryu et al. 2016).

On a molecular level, it has been shown that ABA signaling in endodermis
upregulates the expression of mobile miRNA165/166 and a reduction of
miRNA165/166 repressor ZLL/AGO10 (Bloch, Puli et al. 2019). The elevated
levels of miRNAs suppress the HD-ZIPIII transcription factors that
control the metaxylem cell fate and therefore outer metaxylem cells
often change their identity to protoxylem (Carlsbecker, Lee et al. 2010,
Ramachandran, Wang et al. 2018). The mutant \emph{phb1-d} which is
resistant to miRNA165/166\emph{,} and mutants \emph{scr and shr} which
have a strongly reduced overall levels of miRNA165/166 do not show a
xylem phenotype in response to ABA (Bloch, Puli et al. 2019).
Additionally, a selection of the master regulators of xylem
differentiation, VND1-3\&7, are necessary to properly regulate these
changes in xylem structure (Ramachandran, Augstein et al. 2021). It has
been shown, that VND1-3 are key regulators in the final lignification of
the inner metaxylem under stress conditions, as \emph{vnd1-3} triple
mutants fail to show early differentiation of the inner metaxylem
mediated by ABA application. On the other hand, \emph{vnd7} mutants show
no differences on this trait, but instead show a reduction of the
morphological changes seen in the outer metaxylem. These findings
altogether reinforce a mechanism of direct relation between the water
conducting tissue formation and the water deficit signaling.

Interestingly, that this xylem response seems to be quite conserved
across eudicots both on a molecular and a morphological level, as a
shift from metaxylem to protoxylem can be observed in members of
the\emph{Brassica, Nicotiana, Phtheirospermum,} and \emph{Solanum}
family and a similar increase in expression in VND homologs can be seen
in tomato compared to Arabidopsis (Bloch, Puli et al. 2019,
Ramachandran, Augstein et al. 2021). Furthermore, evidence to the
relation of VNDs and miRNA165/166 to water deficiency in monocots has
given proof that this regulatory pathway could be quite well conserved
among plant species. Mutant lines of a VND homolog, \emph{nut1,} in
maize shows drought stress in normal conditions caused by an
underdeveloped protoxylem in mature plants (Dong, Xu et al. 2020).
Additionally, a knockdown of miRNA166 in rice caused leaf rolling, a
typical drought stress response, when grown normally, and a reduced
transpiration rate, which was caused by a reduced diameter of xylem
cells (Zhang, Zhang et al. 2018).

Besides ABA, jasmonic acid (JA) and cytokinin (CK) have been shown to
play a role in xylem regulation in response to drought. CK is a known
inhibitor of protoxylem differentiation by regulating
pseudophosphotransfer protein AHP6 (Mähönen, Bishopp et al. 2006). It
has been demonstrated that drought lowers the levels of CK while
simultaneously increasing levels of JA (Nishiyama, Watanabe et al. 2011)
(Jang, Chang et al. 2017, Jang and Choi 2018). Interestingly, lower
levels of CK have also been linked to an increased sensitivity to ABA,
suggesting a possible crosstalk between these pathways. However, the
specific roles of ABA and the JA/CK balance seem to be different. While
ABA mostly regulate the differentiation and cell fate of the different
xylem through VNDs and miRNA165/166, the JA/CK balance is regulating the
amount of xylem vessels within the axis (Jang, Chang et al. 2017, Jang
and Choi 2018, Jang, Lee et al. 2018). It has been shown that drought
stress leads to an increase of number of xylem vessels which are
originating from previously undifferentiated procambium cells.
Application of JA shows a similar increase in the number of xylem cells,
while application of CK shows a reduction.

\textbf{3.2 Salt stress}

Another common abiotic stress that is experienced by plants is osmotic
stress due to a saline environment. Comparably to water deficiency, ABA
biosynthesis and signaling are activated by salt stress. However, the
differentiation switch of xylem observed in drought conditions mediated
by ABA is not replicated during the NaCl treatment (Bloch, Puli et al.
2019), showing other unknown elements must play a part in the salt
response. At the same time, it has been shown, that high salinity stress
induces an increased lignification of the xylem tissues in Tomato
plants(Sánchez-Aguayo, Rodríguez-Galán et al. 2004) and other plant
species (Neves, Marchiosi et al. 2010, FERNANDEZ-GARCIA, HERNANDEZ et
al. 2011, Oliveira, Mota et al. 2020, Kong, Mostafa et al. 2021).
However, not much is known on the molecular mechanism of salt-induced
over-lignification.

ACAULIS 5 (ACL5) gene is expressed in the procambium cells and it
encodes a putative spermine synthase that has been isolated in the
mutant screen. Loss-of function \emph{acl5} mutant has an increased
xylem vessel diameter (Shinohara, Okamoto et al. 2019), impaired xylem
patterning and salt hypersensitivity. On the cellular level,
\emph{acl5}mutant shows severe inhibition of the secondary cell wall
formation; the vessels have helical pattern of the cell wall, but not
the pitted pattern and xylem fibers are not produced. The role of ACL5
has been demonstrated in inhibition of the final step of xylem
differentiation- cell death (Muñiz, Minguet et al. 2008). In this mutant
the developing xylem cells undergo early cell death, therefore the
elongation and secondary cell wall formation are prematurely terminated
(Muñiz, Minguet et al. 2008). Several works showed that salt-tolerant
plants have reduced xylem vessel diameter; mutant \emph{acl5} and
quadruple mutant of the \emph{SAC51} gene family have increased xylem
diameter and show hypersensitivity to salt (Shinohara, Okamoto et al.
2019). Taken together, the abiotic stresses impact on xylem patterning
through modulating hormonal signaling and affecting the structure of
conducting elements- from patterning the secondary cell wall to defining
the thickness of the cell wall and vessel diameter. The molecular
mechanisms of stress-regulated xylem patterning is an exceptionally
important topic especially in the light of global climate change and we
hope near future will bring more discoveries in this field.

\textbf{4. Wilt pathogens and their impact on xylem}

On top of abiotic factors that affect plant growth, multiple pathogens
and pests interfere with plant development and often cause plant death.
Vascular system is an attractive target for many pathogens while wilt
pathogens that attack xylem tissues are among the most harmful for plant
health (Yadeta and Thomma 2013). This group of pathogens are represented
by microscopic fungi (for instance, \emph{Fusarium oxysporum}) or
bacteria (for instance, \emph{Xylella fastidiosa}) and can lead to
wilting and even death of the plant. The invasion of these pathogens
often happens through the root system, where they enter the epidermis,
continue through cortex and endodermis reaching the xylem. In xylem
these pathogens proliferate and spread to the above ground organs (Bae,
Han et al. 2015). Another strategy is used by vascular bacteria, for
instance, \emph{Xylella fastidiosa}, that directly inoculated into the
xylem tissue by insects that attack the plant (Wang, Lee et al. 2017).
Remarkably, the strategies to resist wilt pathogens are often associated
with xylem capacity to recognize the pathogen and to block the infection
by producing polymers (lignin, suberin), or secreting gels and formation
tyloses (reviewed in (Kashyap, Planas-Marques et al. 2021)) (Figure 3).
While pathogen recognition is a highly advanced field today, our
understanding of the xylem responses to compartmentalize the pathogen
mainly relays on the anatomical studies of the infected tissues and some
recent proteomics and transcriptomics studies (Hu, Puri et al. 2019,
Xiong, Sun et al. 2021).

After successful blocking the infected region of xylem, plants often
need to re-connect the network by creating new conducting elements from
the adjacent parenchyma cells. Remarkably, the induction of physical
barriers and re-wiring require a highly coordinated and timely response
in xylem tissue; often the susceptible plants also produce polymers or
gels and tyloses to stop the propagation of the pathogen, but not in a
local or rapid manner and then the infection takes over (Planas-Marquès,
Kressin et al. 2020). Studying the molecular mechanisms and the genetic
basis of re-connecting of xylem upon infection is essential and needs
the combined effort of developmental biologists and plant pathologists.
Developing strategies for crop plants that recognize and respond rapidly
and locally to stop the pathogen will bring promising solutions for the
future.

\textbf{5. Perspectives in Xylem phenotyping and water use modeling}

Plants consume large amounts of water for their metabolism and even more
water they lose during transpiration. Therefore, plant water management,
including the uptake, the hydraulics within the xylem system and
transpiration through stomata impact the global water cycle, the
agriculture and our ecosystems (Schlesinger and Jasechko 2014). Xylem
system in plants exploits a passive mechanism of water transport from
the root to the shoot. Because this most essential for plants process
relays on water movement within dead capillaries, two large areas of
research deal with how the water conducting tissue is formed and can be
modified (vascular development) and how water moves inside the xylem
network (plant hydraulics). While the developmental biologists look into
gene regulatory networks, anatomy and cell biology, the plant hydraulics
focuses on biophysics of water flow, xylem embolism, hydraulic
conductance and vulnerability (Venturas, Sperry et al. 2017). In our
opinion, in the future more collaboration between these two fields will
bring valuable advances in the understanding of water transport. We
believe, such collaborations will be essential for finding new solutions
in developing better crops. Using the methodologies of both areas of
research, it will be possible to come up for example with ``Root Xylem
Index'' that could be used to assess the capability of root xylem
network of the specific plant species and varieties. This index can be
used later by farmers to select the best cultivars or varieties for a
given field and conditions. In the recent study on maize roots five
cultivars of maize were grown in pots and later used for anatomical
analysis and modelling. The authors created a high-resolution root
system hydraulic atlases for maize plant (Heymans, Couvreur et al.). In
this study among the other parameters, five were related to the
vasculature. This work is a nice example of modelling water transport
combining the anatomical traits and mathematics and this protocol for
assessment of root hydraulic capability can be used with many other
species (Heymans, Couvreur et al.). The microscopic differences in the
structure of xylem cells can be later used to estimate global water use
properties of the plant. This knowledge will be essential in designing
crops with optimal xylem system.

\textbf{Figure legends}

\textbf{Figure 1. Xylem formation: from the precursors to functional
capillaries.} A. The ontogeny of xylem in early Arabidopsis embryo. B.
The on-set of primary xylem differentiation in Arabidopsis and Tomato
roots. The illustration shows the gradual lignification of the
protoxylem and later metaxylem cells and below the confocal images show
a region where the protoxylem is already lignified. The confocal images
were done with Zeiss780, the Calcofluor staining decorates cell walls
and in red- Basic Fuchsin staining shows the lignification. The scale
bar corresponds to 50mm.

\textbf{Figure 2.} \textbf{Xylem pattern formation.} A. In the root tip
the xylem pole is located in the center of the vascular cylinder, with
three metaxylem cells flanked by protoxylem. B. Cellular changes during
proto- and metaxylem differentiation. C. The key transcription factors
mediating xylem differentiation. D. Radial patterning in xylem mediated
by HD-ZIP III transcription factors and mobile miRNAs.

\textbf{Figure 3.}~\textbf{Environmental stresses impact on xylem
patterning.~}Xylem pathogens infect functional vessels, that can lead to
tyloses (cell outgrowth of the xylem parenchyma), production of polymers
for vascular coating and induction of new xylem vessels in adjacent
tissue to reconnect the vascular system. Under drought conditions, ABA
induces miRNAs production that represses HD-ZIP III transcription
factors leading to developing more protoxylem cell files replacing
metaxylem. In addition, ABA signaling induces early lignification of the
inner metaxylem. Salt stress leads to increased lignification and
decreased diameter of xylem vessels.

\textbf{Author contributions:} The review was written and edited by SC
and OH.

\textbf{Funding:} The research on xylem development in Arabidopsis and
Tomato roots in the lab of OH is funded by SNSF AMBIZIONE Grant
(PZ00P3\_179745), SNSF COST Grant (IZCOZ0\_189892) and supported by the
additional funding from the Department of Biology, University of
Fribourg.

\textbf{Acknowledgements:} we would like to acknowledge Olivier Amrein
for the help in preparing the illustrations.

\textbf{Conflict of interest:} The authors declare no conflict of
interest.

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