This special issue of Journal of Experimental Botany focuses on the developmental mechanisms required to generate plant vascular tissue. The focus is Arabidopsis, including the three models for initial patterning involving the interaction of auxin and cytokinin, and going on to look at expansion and differentiation into xylem and phloem. Bryophyte and tree models are also considered, as well as new techniques for analyzing the vasculature of mature plants.

There are many advantages to using plant vascular tissue as a model for studying developmental biology. These include a very high level of tissue organization that is apparent both early in development, where highly coordinated cell divisions in the embryo are required to specify the vascular tissue (Berleth and Jurgens, 1993), and during secondary growth, where highly oriented cell divisions in the cambium, a bifacial meristem, drive radial growth and expansion (Chaffey et al., 2002) (Box 1). Differentiated tissues, the xylem and phloem, are derived from divisions in vascular meristems. Consequently studying vascular tissue formation takes in classic developmental biology themes of cell division, tissue organization and differentiation.

Box 1. Examples of monocot and dicot vascular tissue

Monocot vascular tissue such as that of Sorghum bicolor (A) is present in bundles (arrowheads) arranged along the radial axis of the stem. Mature vascular bundles are present towards the centre of the stem, while younger bundles are initiated close to the epidermis. Dicot vascular tissue in mature plants is often derived from a continuous ring of cambium (B; arrowhead), such as that found in the Arabidopsis hypocotyl. ph, phloem; x, xylem. Scale bar = 50 μm.

 

Ohtani et al. (2017) review the evolution of water and nutrient transport systems in bryophytes through to the vascular system widely recognizable in higher plants. Terrestrial plants require water and nutrients from the soil and sunlight captured in aboveground organs for growth and development. There would have been considerable selective pressure on early land plants for a transport mechanism that allowed all cells in the plant to access these resources. Vascular systems have enabled plants to increase in size through evolutionary time by facilitating the transport of these resources around the plant and are consequently pivotal to higher plant evolution. Furthermore, innovations such as the rigid secondary cell wall, present in the water-conducting cells of the xylem, enable these vessels to withstand the negative pressures of water transport, but also provide the support allowing increases in plant height to improve light capture. Ohtani et al. (2017) also review our knowledge of how transcription factors regulate vascular differentiation, and explore the role these transcription factors may have in driving the evolution of vascular systems in lower plants.

Pattern specification and expansion

The vascular tissue is specified early in development, and a number of recent papers have focused on how the vascular systems that have evolved in higher plants initiate and expand. In both the embryo and the root of Arabidopsis, a central xylem axis is specified with phloem poles on either side. Several groups have taken a mathematical modelling approach to address the question of how this pattern arises, and in the last couple of years three models have emerged that support the idea that an interaction of auxin and cytokinin probably underpins pattern generation in the root and embryo (De Rybel et al., 2014; Muraro et al., 2014; El-Showk et al., 2015). These models build on our understanding of the roles of auxin and cytokinin and their transport in determining early vascular pattern, gained from genetic and cell biology data over the past decade (Hardtke and Berleth, 1998; Mähönen et al., 2006; Izhaki and Bowman, 2007; Ilegems et al., 2010; Bishopp et al., 2011a; Bishopp et al., 2011b; De Rybel et al., 2013; Ohashi-Ito et al., 2013). However, the wiring within these models is varied. For example, that put forward by Muraro et al. (2014) also incorporates an interaction between the class III homeodomain-leucine zipper (HD-Zip III) transcription factor PHABULOSA (PHB) and cytokinin, an interaction explored in this special issue (Ramachandran et al., 2017). In all cases the models make novel predictions that have subsequently been validated, so certainly all expand our understanding of early vascular development.

How does one compare the differences in the model outputs, and what are the implications of such comparisons? In this special issue, the groups behind the models report further comparisons – simulations have been rerun through each model using the data used to generate the other complementary models (De Rybel et al., 2014; Muraro et al., 2014; El-Showk et al., 2015). There were some disagreements in the outputs, most notably around cytokinin gradients, indicating that further experiments are required. Nevertheless all three models support the interaction of auxin and cytokinin as a plausible system for generating early vascular pattern (Mellor et al., 2017). While these hormone interactions are responsible for generating pattern, they are underpinned by a network of interacting factors, dominated by helix-loop-helix transcription factors, TARGET OF MONOPTEROS 5 (TMO5) (Schlereth et al., 2010), LONESOME HIGHWAY (LHW) (Ohashi-Ito and Bergmann, 2007), SUPRESSOR OF ACAULIS51 (SAC51) (Imai et al., 2006), and SAC51-LIKE (SACL) (Cai et al., 2016), that act downstream of auxin signalling and influence cytokinin activity (reviewed in Campbell and Turner, 2017).

Following specification of the initial pattern, the vasculature rapidly expands to match plant growth. This expansion is underpinned by cell division in the vascular meristems (cambium or procambium), and these cells subsequently differentiate into xylem and phloem. The meristem is maintained by balancing cell division and differentiation. A series of receptor kinases is critical to maintaining this balance, with expression in differing domains of the vasculature. PHLOEM INTERCALATED WITH XYLEM (PXY) is a receptor-like kinase (RLK) that is expressed predominantly on the side of the cambium adjacent to the xylem, and it functions to both promote cell division and repress xylem identity from the cambium (Etchells et al., 2016). The phloem side of the cambium is regulated by a recently characterized RLK, MORE LATERAL GROWTH1 (MOL1), that is related to PXY. In contrast to PXY, MOL1 acts to repress cell division (Gursanscky et al., 2016). A further family of RLKs, members of the ERECTA (ER) family (ERf), also regulate cell division in a number of contexts including the vasculature (Uchida and Tasaka, 2013). ER is expressed in the phloem, and it acts redundantly with its closest homologue, ERL1, to control vascular proliferation. While the ligand for MOL1 is currently unknown, those for the ERf RLKs CHALLAH/EPIDERMAL PATTERNING FACTOR LIKE6 (EPFL6), CHALLAH-LIKE1 (CLL1)/EPFL5 and CLL2/EPFL4 (Abrash et al., 2011) are expressed in the endodermis (Uchida et al., 2012). The PXY ligand, TDIF, is derived from genes expressed in the phloem. Therefore, differing RLKs mark different vascular domains, as do their respective ligands. These non-cell autonomous relationships and distinct expression domains hint at a role in vascular organization, and these themes of proliferation and organization are explored in depth in Tameshige et al. (2017) and Turner and Campbell (2017).

Maintenance of vascular meristems is clearly under tight genetic control. In xylem initials, this differentiation is controlled by a very large gene regulatory network (Taylor-Teeples et al., 2015), in which HD-Zip III genes are prominent (Zhong and Ye, 1999; Baima et al., 2001; Ohashi-Ito et al., 2002; Ochando et al., 2008; Baima et al., 2014; Du et al., 2015). Ramachandran et al. (2017) explore the role that HD-Zip III genes play in vascular patterning in many contexts, including in early patterning of the root xylem axis, radial patterning of vascular bundles in the stem, and regulation of cell wall polymer deposition in the xylem. In comparison to xylem specification, less is known about how the phloem cell types are specified and differentiated. However, following identification of BREVIS RADIX (BRX) (Mouchel et al., 2004) and OCTOPUS (OPT) (Truernit et al., 2012), genes that control the timing and rate of sieve element differentiation, as well as their regulators, the ligand receptor pair CLAVATA3/ENDOSPERM SURROUNDING REGION-related 45 (CLE45) and BARELY ANY MERISTEM3 (BAM3), a picture is beginning to emerge (Rodriguez-Villalon et al., 2014). In this issue, Otero and Helariutta (2017) focus on companion cell specification, and describe the critical function of these cells in loading nutrients and mobile signals, such as FLOWERING TIME (FT), to neighbouring sieve elements for transport.

Trees and techniques

Many of the discoveries described above focus on developmental mechanisms characterized in Arabidopsis. While this small annual remains unsurpassed in the plant kingdom as a tool for gene discovery, there remains a challenge in assessing the gene and hormone networks that have been uncovered in it in different contexts. However, a system in which this has been performed effectively is wood deposition in poplar trees. Comparisons between radial growth in the Arabidopsis hypocotyl and in particular poplar trees have been described; however, tree models are also essential for investigating aspects of growth that cannot be addressed in annual plants. Here, Bhalerao and Fischer (2017) describe vascular development from this perspective, reviewing how gene and hormone networks respond during entry into cambial dormancy over winter and exit into growth in spring, and exploring our understanding of the genetic basis of extreme longevity of cambium cells in some trees.

While the advantages of using vascular tissue as a developmental model are mentioned at the beginning of this article, one major drawback to studying vascular tissue – particularly after pattern has been established late in development, during secondary growth – is that rapid radial growth makes live imaging unfeasible. The vascular cell divisions and differentiation process occur many layers into the tissue. Wunderling et al. (2017) review recently described methods for analyzing the vasculature in mature plants. Such innovations will enable the generation of more high quality quantitative data, which will be critical in placing new discoveries into context as the field expands.

Perspectives

All the reviews in this special issue demonstrate that our understanding of the vascular meristem and the differentiation of the xylem and phloem produced from it has improved dramatically. There is, however, no review on vascular development in monocots even though they are by far and away the most important crop species globally. Vascular development in monocots is very distinctive and quite different to that of dicots (Box 1), yet despite their importance to global food security, our understanding of vascular development in these species lags far behind. This is partially a consequence of the fact that much of our current knowledge has been obtained from studying the genetically tractable Arabidopsis, or by analyzing the highly organized arrangement of tissues seen in secondary growth. However, it is still unclear how many of the important genes identified as important in dicot vascular development function in the same way in monocots. Whilst this clearly has the potential to be an interesting study in evolution and development, it is imperative that our understanding of vascular developments in monocots must improve in order to establish whether altering vascular tissue development can contribute to producing better, more resilient crop plants better able to meet the challenges associated with population growth coupled with climate change.

References

Abrash
EB
Davies
KA
Bergmann
DC
.
2011
.
Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand–receptor interactions
.
The Plant Cell
 
23
,
2864
2879
.
Baima
S
Forte
V
Possenti
M
Peñalosa
A
Leoni
G
Salvi
S
Felici
B
Ruberti
I
Morelli
G
.
2014
.
Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module
.
Molecular Plant
 
7
,
1006
1025
.
Baima
S
Possenti
M
Matteucci
A
Wisman
E
Altamura
MM
Ruberti
I
Morelli
G
.
2001
.
The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems
.
Plant Physiology
 
126
,
643
655
.
Berleth
T
Jurgens
G
.
1993
.
The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo
.
Development
 
118
,
575
587
.
Bhalerao
RP
Fischer
U
.
2017
.
Environmental and hormonal control of cambial stem cell dynamics
.
Journal of Experimental Botany
 
68
,
79
87
.
Bishopp
A
Help
H
El-Showk
S
Weijers
D
Scheres
B
Friml
J
Benková
E
Mähönen
AP
Helariutta
Y
.
2011
a.
A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots
.
Current Biology
 
21
,
917
926
.
Bishopp
A
Lehesranta
S
Vatén
A
Help
H
El-Showk
S
Scheres
B
Helariutta
K
Mähönen
AP
Sakakibara
H
Helariutta
Y
.
2011
b.
Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem
.
Current Biology
 
21
,
927
932
.
Cai
Q
Fukushima
H
Yamamoto
M
Ishii
N
Sakamoto
T
Kurata
T
Motose
H
Takahashi
T
.
2016
.
The SAC51 family plays a central role in thermospermine responses in Arabidopsis
.
Plant and Cell Physiology
 
57
,
1583
1592
.
Turner
S
Campbell
L
.
2017
.
Regulation of vascular cell division
.
Journal of Experimental Botany
 
68
,
27
43
.
Chaffey
N
Cholewa
E
Regan
S
Sundberg
B
.
2002
.
Secondary xylem development in Arabidopsis: a model for wood formation
.
Physiologia Plantarum
 
114
,
594
600
.
De Rybel
B
Adibi
M
Breda
AS
et al
.
2014
.
Integration of growth and patterning during vascular tissue formation in Arabidopsis
.
Science
 
345
,
1255215-1
1255215-8
.
De Rybel
B
Möller
B
Yoshida
S
Grabowicz
I
Barbier de Reuille
P
Boeren
S
Smith
RS
Borst
JW
Weijers
D
..
2013
.
A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis
.
Developmental Cell
 
24
,
426
437
.
Du
Q
Avci
U
Li
S
Gallego-Giraldo
L
Pattathil
S
Qi
L
Hahn
MG
Wang
H
.
2015
.
Activation of miR165b represses AtHB15 expression and induces pith secondary wall development in Arabidopsis
.
The Plant Journal
 
83
,
388
400
.
El-Showk
S
Help-Rinta-Rahko
H
Blomster
T
Siligato
R
Marée
AFM
Mähönen
AP
Grieneisen
VA
.
2015
.
Parsimonious model of vascular patterning links transverse hormone fluxes to lateral root initiation: auxin leads the way, while cytokinin levels out
.
PLoS Computational Biology
 
11
,
e1004450
.
Etchells
JP
Smit
ME
Gaudinier
A
Williams
CJ
Brady
SM
.
2016
.
A brief history of the TDIF-PXY signalling module: balancing meristem identity and differentiation during vascular development
.
New Phytologist
 
209
,
474
484
.
Gursanscky
NR
Jouannet
V
Grünwald
K
Sanchez
P
Laaber-Schwarz
M
Greb
T
.
2016
.
MOL1 is required for cambium homeostasis in Arabidopsis
.
The Plant Journal
 
86
,
210
220
.
Hardtke
CS
Berleth
T
.
1998
.
The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development
.
EMBO Journal
 
17
,
1405
1411
.
Ilegems
M
Douet
V
Meylan-Bettex
M
Uyttewaal
M
Brand
L
Bowman
JL
Stieger
PA
.
2010
.
Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation
.
Development
 
137
,
975
984
.
Imai
A
Hanzawa
Y
Komura
M
Yamamoto
KT
Komeda
Y
Takahashi
T
.
2006
.
The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene
.
Development
 
133
,
3575
3585
.
Izhaki
A
Bowman
JL
.
2007
.
KANADI and Class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis
.
The Plant Cell
 
19
,
495
508
.
Mähönen
AP
Bishopp
A
Higuchi
M
Nieminen
KM
Kinoshita
K
Törmäkangas
K
Ikeda
Y
Oka
A
Kakimoto
T
Helariutta
Y
.
2006
.
Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development
.
Science
 
311
,
94
98
.
Mellor
N
Adibi
M
El-Showk
S
De Rybel
B
King
J
Mähönen
AP
Weijers
D
Bishopp
AB
.
2017
.
Theoretical approaches to understanding root vascular patterning: a consensus between recent models
.
Journal of Experimental Botany
 
68
,
5
16
.
Mouchel
CF
Briggs
GC
Hardtke
CS
.
2004
.
Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root
.
Genes & Development
 
18
,
700
714
.
Muraro
D
Mellor
N
Pound
MP
et al
.
2014
.
Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots
.
Proceedings of the National Academy of Sciences, USA
 
111
,
857
862
.
Ochando
I
González-Reig
S
Ripoll
JJ
Vera
A
Martínez-Laborda
A
.
2008
.
Alteration of the shoot radial pattern in Arabidopsis thaliana by a gain-of-function allele of the class III HD-Zip gene INCURVATA4
.
The International Journal of Developmental Biology
 
52
,
953
961
.
Ohashi-Ito
K
Bergmann
DC
.
2007
.
Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY
.
Development
 
134
,
2959
2968
.
Ohashi-Ito
K
Demura
T
Fukuda
H
.
2002
.
Promotion of transcript accumulation of novel Zinnia immature xylem-specific HD-Zip III homeobox genes by brassinosteroids
.
Plant and Cell Physiology
 
43
,
1146
1153
.
Ohashi-Ito
K
Matsukawa
M
Fukuda
H
.
2013
.
An atypical bHLH transcription factor regulates early xylem development downstream of auxin
.
Plant and Cell Physiology
 
54
,
398
405
.
Ohtani
M
Akiyoshi
N
Takenaka
Y
Sano
R
Demura
T
.
2017
.
Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation
.
Journal of Experimental Botany
 
68
,
27
43
.
Otero
S
Helariutta
Y
.
2017
.
Companion cells: a diamond in the rough
.
Journal of Experimental Botany
 
68
,
71
78
.
Ramachandran
P
Carlsbecker
A
Etchells
JP
.
2017
.
Class III HD-ZIPs govern vascular cell fate: an HD view on patterning and differentiation
.
Journal of Experimental Botany
 
68
,
55
69
.
Rodriguez-Villalon
A
Gujas
B
Kang
YH
Breda
AS
Cattaneo
P
Depuydt
S
Hardtke
CS
.
2014
.
Molecular genetic framework for protophloem formation
.
Proceedings of the National Academy of Sciences, United States of America
 
111
,
11551
11556
.
Schlereth
A
Moller
B
Liu
W
Kientz
M
Flipse
J
Rademacher
EH
Schmid
M
Jurgens
G
Weijers
D
.
2010
.
MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor
.
Nature
 
464
,
913
916
.
Tameshige
T
Ikematsu
S
Torii
K
Uchida
N
.
2017
.
Stem development through vascular tissues: EPFL-ERECTA family signaling that bounces in and out of phloem
.
Journal of Experimental Botany
 
68
,
45
53
.
Taylor-Teeples
M
Lin
L
de Lucas
M
et al
.
2015
.
An Arabidopsis gene regulatory network for secondary cell wall synthesis
.
Nature
 
517
,
571
575
.
Truernit
E
Bauby
H
Belcram
K
Barthélémy
J
Palauqui
J-C
.
2012
.
OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana
.
Development
 
139
,
1306
1315
.
Uchida
N
Lee
JS
Horst
RJ
Lai
H-H
Kajita
R
Kakimoto
T
Tasaka
M
Torii
KU
.
2012
.
Regulation of inflorescence architecture by intertissue layer ligand–receptor communication between endodermis and phloem
.
Procedings of the National Academy of Sciences, USA
 
109
,
6337
6342
Uchida
N
Tasaka
M
.
2013
.
Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases
.
Journal of Experimental Botany
 
64
,
5335
5343
Wunderling
A
Ben-Targem
M
Barbier de Reuille
P
Ragni
L
.
2017
.
Secondary growth quantification: problematics and novel tools
.
Journal of Experimental Botany
 
68
,
89
95
.
Zhong
R
Ye
Z-H
.
1999
.
IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein
.
The Plant Cell
 
11
,
2139
2152
.

Author notes

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Comments

0 Comments