Article
Reference
Polarized transport across root epithelia
RAMAKRISHNA, Priya, BARBERON, Marie
Abstract
Plant roots explore the soil to acquire water and nutrients which are often available at concentrations that drastically differ from the plant's actual need for growth and development.
This stark difference between availability and requirement can be dealt with owing to the root's architecture as an inverted gut. In roots, the two epithelial characteristics (selective acquisition and diffusion barrier) are split between two cell layers: the epidermis at the root periphery and the endodermis as the innermost cortical cell layer around the vasculature. Polarized transport of nutrients across the root epithelium can be achieved through different pathways: apoplastic, symplastic, or coupled transcellular. This review highlights different features of the root that allow this polarized transport. Special emphasis is placed on the coupled transcellular pathway, facilitated by polarized nutrient carriers along root cell layers but barred by suberin lamellae in endodermal cells.
RAMAKRISHNA, Priya, BARBERON, Marie. Polarized transport across root epithelia. Current Opinion in Plant Biology, 2019, vol. 52, p. 23-29
DOI : 10.1016/j.pbi.2019.05.010
Available at:
http://archive-ouverte.unige.ch/unige:145014
Disclaimer: layout of this document may differ from the published version.
Polarized transport across root epithelia Priya Ramakrishna 1, Marie Barberon1,#
1Department of Botany and Plant Biology, University of Geneva, 30 Quai Ernest Ansermet, 1211 Geneva, Switzerland
#Corresponding author
Marie Barberon – marie.barberon@unige.ch
Abstract
Plant roots explore the soil to acquire water and nutrients which are often available at concentrations that drastically differ from the plant’s actual need for growth and development. This stark difference between availability and requirement can be dealt with owing to the root’s architecture as an inverted gut. In roots, the two epithelial characteristics (selective acquisition and diffusion barrier) are split between two cell layers: the epidermis at the root periphery and the endodermis as the innermost cortical cell layer around the vasculature. Polarized transport of nutrients across the root epithelium can be achieved through different pathways: apoplastic, symplastic, or coupled transcellular. This review highlights different features of the root that allow this polarized transport. Special emphasis is placed on the coupled transcellular pathway, facilitated by polarized nutrient carriers along root cell layers but barred by suberin lamellae in endodermal cells.
Highlights
• The plant root can be functionally likened to an inverted gut epithelium
• The absorptive surface formed by the epidermis and root hairs is responsive to nutrient availability
• Polar localization of nutrient carriers across root cell layers allows directional cell-to-cell transport
• The endodermis forms bidirectional barriers with tight control of apoplastic and transcellular nutrient transport pathways
• Suberin lamellae are highly plastic in response to nutrients, hormones, and in response to Casparian strip defects
Introduction 1
Multicellularity enables cell specialization. It relies on communication, coordination and transport 2
between differentiated cells that are organized into tissues of specific function. Cell-to-cell transport 3
and communication are particularly important for the uptake and transport of nutrients from one 4
part of an organism to another. In plants, the nutrients present in the soil are acquired by roots and 5
transported from the root periphery (outside), to the central vasculature, where they are loaded into 6
xylem vessels (inside) to be transported to the aerial parts. Plant roots consists of concentric layers of 7
cells that surround the vasculature. The outermost epidermal layer with its root hairs form the 8
surface for absorption, followed by cortical cell layers with the innermost cortical layer, the 9
endodermis, forming diffusion barriers (Figure 1A). Importantly, these root cell layers are polarized.
10
An increasing number of nutrient carriers are shown to localize to the outer (soil facing) or inner 11
(stele facing) plasma membrane domain, which allows polarized nutrient transport across root 12
layers. Together, these features of the root allow for three nutrient uptake scenarios: the apoplastic 13
pathway, passive diffusion through extracellular space in the cell wall barred by Casparian strips; the 14
symplastic pathway, cell-to-cell transport achieved through plasmodesmata (cytoplasmic 15
connections between adjacent cells); and the coupled transcellular pathway, facilitated by polarized 16
influx and efflux carriers along root cell layers and barred by suberin lamellae (Figure 1C) [1–4]. 17
Similarly, and more widely known, in animals, the specialized epithelial cells of the gut facilitate 18
polarized acquisition of nutrients from the intestinal lumen (outside) to the blood vessels (inside).
19
This specific function relies on the plasma membrane of the epithelial cells being polarized and 20
organized into two discrete apical and basolateral regions with specialized functions (Figure 1B). The 21
apical surface of epithelial cells form numerous finger-like protrusions called microvilli that increase 22
the surface for absorption. Influx and efflux carriers localized to the apical or basolateral regions 23
respectively, allow for polarized acquisition of nutrients through the so-called transcellular pathway.
24
The polarity of the epithelial cells is maintained by the presence of tight junctions, multiprotein 25
complexes that seal the space between epithelial cells, and control the paracellular pathway (Figure 26
1D) [5]. Functionally, the plant root can therefore be likened to an inverted intestinal gut epithelium 27
with the epithelial functions (selective acquisition and diffusion barriers), split across the root cell 28
layers [3,6–8].
29
In this review, we highlight recent advances in root hair dynamics, polarity of nutrient carriers, and 30
endodermal barriers, the three components essential for the polarized uptake of nutrients in the 31
root epithelium. The review will focus mainly on Arabidopsis where most of the genetic evidences 32
were obtained. However, it is important to note that the Arabidopsis root is a simplified system 33
without an exodermis, a layer formed below the epidermis with structural similarity to endodermis, 34
and expected functional similarity as an additional barrier for nutrient transport in the roots [9].
35
Understanding plant nutrition at the organismal level requires insight into subcellular processes, cell 36
differentiation and action of nutrient carriers at the tissue level. Much of the evidence presented 37
here are based on classic physiological assays combined with advancements in live-imaging 38
approaches and functional genetics.
39 40
The root hairs as a surface of absorption 41
Root hairs are specialized cells in the root epidermis that extend the radial reach of roots. Nutrients 42
taken up through root hairs are subsequently transported to the vasculature through symplastic or 43
coupled transcellular pathways (Figure 1C). Fitting with their role in nutrient uptake, most of the 44
main carriers for mineral acquisition at the root periphery are expressed in root hairs [10,11]. In 45
various crops, longer root hairs were shown to associate with increased absorption of phosphate and 46
potassium [12–14]. In Arabidopsis, several root-hair-less mutants have been reported to be affected 47
in the acquisition of nutrients such as phosphate, potassium, iron, zinc, copper and calcium 48
[10,15,16]. Patch-clamp assays in living root hairs or root hair protoplasts demonstrated the function 49
of root hairs in ion uptake, especially for potassium and calcium [17–20]. X-ray Tomographic 50
Microscopy of wheat root hairs in soil combined with modeling of phosphate uptake predicted the 51
important role of root hairs during phosphate depletion from the soil [21].
52
Root hair development consists of two major steps: cell fate determination which produces hair or 53
non-hair epidermal cells, and differentiation where root hairs initiate and elongate to the outer 54
domain (Figure 1A) [22]. Nutrient availability is a well-known parameter that impacts the shape, 55
positioning and number of root hairs [23], and the epidermal cell differentiation is particularly 56
responsive to availability of iron, zinc, phosphate and manganese [24–27]. Root hair response to 57
inorganic phosphate availability has been well studied with phosphate deficiency leading to an 58
increase in root hair length and density [23–25,28,29]. Recently, a new microfluidics based platform 59
called Dual-flow-RootChip allowed localized application of stress and subsequent live visualization of 60
responses in parallel in multiple living Arabidopsis roots [30]. Using this method, an unexpected cell- 61
autonomous adaptation of root hair development under asymmetric phosphate perfusion was 62
characterized with an upregulation of root hair growth on the side exposed to high phosphate. These 63
advances highlight the importance of root hair in nutrient uptake and the need to uncover the 64
underlying transport mechanisms.
65
Polarized nutrient carriers 66
Apico-basal polarity of influx and efflux carriers is paramount for the transcellular transport of 67
nutrients in animal epithelia. In plants, the feature had been overlooked for several years, but has 68
recently gained an increasing interest reviewed in [4,6,22]. In roots, nutrient carriers show polar 69
localization to either to the outer soil-facing domain, or the inner vasculature-facing domain. This 70
allows directional cell-to-cell transport of nutrients across the different root cell layers (coupled 71
transcellular pathway) (Figure 1C). This has been particularly well demonstrated in rice, with influx 72
and efflux carriers located to the outer and inner domain, respectively of endodermal and exodermal 73
cells. It applies as well to the pair of silicon transporters- Lsi1 (Low-Silicon 1, influx channel) and Lsi2 74
(Low-Silicon 2, exporter), and the pair of manganese transporters NRAMP5 (Natural Resistance- 75
Associated Macrophage Protein 5, influx transporter) and MTP9 (Metal Tolerance Protein 9, efflux 76
transporter) [31–34]. In Arabidopsis, the same dual polarity was demonstrated for the pair of boron 77
transporters NIP5;1 (Nodulin 26-like Intrinsic Protein 5;1, boric influx channel), and BOR1/BOR2 78
(boric acid/borate exporters), localized respectively to the outer or inner domains of epidermal cells, 79
and the pair of NIP5;1 and BOR1 localized respectively to the outer and inner domain of endodermal 80
cells (Figure 2) [35–39]. The example with boron transporters illustrates that lateral polarity of 81
nutrient carriers is not restricted to endodermal/exodermal cells and emphasizes the existence of a 82
coupled transcellular pathways for nutrients across root cell layers. This is further illustrated by the 83
localization of the high-affinity nitrate transporter NRT2;4 and the metal transporter IRT1 (IRON 84
REGULATED TRANSPORTER 1) to the outer domain of epidermal cells [40–42]. However, in these 85
cases a corresponding efflux transporter localizing to the inner domain remains to be identified 86
(Figure 2).
87
The mechanisms that control this polarity have been particularly characterized for BOR1 and IRT1. In 88
situ imaging of these two transporters showed that their plasma membrane localization is regulated 89
by the availability of their respective substrates [37,39,41–46]. The underlying mechanisms for BOR1 90
and IRT1 polar localization has been recently reviewed extensively [22,47,48]. These works identified 91
mutations that interfere with polarity to demonstrate its importance in nutrient transport across 92
root cell layers. This has been suggested for the transporter IRT1 where analysis of plants with apolar 93
localization of IRT1 was accompanied by a reduction in metal acquisition [41]. More recently, this 94
function was well demonstrated for boron transport through a combination of modeling and 95
experimental analysis of mutants affected in BOR1 or NIP5;1 polarity [46,49,50].
96 97
Diffusion barriers in the endodermis 98
Nutrients transported from the root periphery to the vasculature need to enter endodermal cells 99
through a short symplastic or transcellular pathway. This is due to the presence of Casparian strips, 100
lignin deposits between adjacent endodermal cells, that seal the apoplastic space to form the first 101
stage of endodermal differentiation [51–54]. Nutrient uptake in endodermal cells are tightly 102
controlled, suggested to be facilitated by nutrient carriers in the outer domain of endodermal cells 103
(most of which remain to be identified and characterized), and blocked by the presence of suberin 104
lamellae. Suberin lamellae are a secondary cell wall deposition of hydrophobic polymers. They 105
establish a diffusion barrier for the transcellular pathway and form the second stage of endodermal 106
differentiation (Figure 1A) [53,55]. Intriguingly, some individual endodermal cells present at the 107
xylem poles remained non-suberized [56,57]. These cells, called passage cells, are hypothesized to 108
serve as points for nutrient entry into the vasculature, which is supported by the expression of 109
phosphate exporters that remain specific to these non-suberized cells [56,58]. To be validated this 110
model would benefit from extensive characterization of nutrient carriers expression and activity in 111
suberized or non-suberized endodermal tissues.
112
Recently, efforts aimed to characterize the physiological effects of defective endodermal barriers.
113
Surprisingly, impaired Casparian strips or absence of suberin lamellae led to moderate but specific 114
defects in nutrient accumulation [55,59–64]. The absence of a massive nutrient overaccumulation in 115
plants without functional barriers is counterintuitive. However, it reflects the crucial regulatory role 116
of the endodermis as a bidirectional barrier that not only blocks nutrient entry to, but prevents 117
leakage from the vasculature [1,65]. This was in particular suggested for potassium, shown to 118
accumulate principally in the central vasculature and at lower levels in plants with defective 119
endodermal barriers [55,61,66].
120
Illustrating the fundamental role of endodermal barriers, most Casparian strip defective mutants 121
compensate with ectopic deposition of lignin and suberin in the endodermis [60,62,63,67]. The 122
underlying mechanism involves two diffusible peptides produced in the vasculature (Casparian Strip 123
Integrity Factor 1 and 2, CIF1 and CIF2), and their endodermal leucine-rich-repeat receptor-like 124
kinase (LRR_RLK) SCHENGEN3 (SGN3, also known as GASSHO1) and cytoplasmic receptor like kinase 125
SGN1 localizing around the Casparian strip domain and to the outer plasma membrane side of 126
endodermal cells respectively [52,61,68,69]. Current models suggest physical separation of the 127
receptors and ligands by functional Casparian strips. Their interaction at the outer apoplastic domain 128
of endodermal cells is possible only when Casparian strips are impaired [1,54,68]. Moreover, 129
endodermal suberization is regulated by a multitude of abiotic stress including drought, 130
waterlogging, salt stress or cadmium exposure in many plant species [55,70–75]. In Arabidopsis, 131
action of the two hormones abscisic acid (ABA) and ethylene [55,56,64,75]. This plasticity of suberin 133
formation in response to mineral deficiencies represents a mechanism to fine-tune nutrient 134
acquisition in response to the plant’s demand.
135 136
Conclusion 137
Altogether, the work presented here highlight the interest to develop and apply live-imaging 138
approaches to study mechanisms of radial nutrient transport in roots. These approaches are 139
particularly relevant for root hairs, nutrient carriers, and endodermal barriers in relation to nutrient 140
availability [66,76–80]. We can predict that further development of techniques and markers to allow 141
live imaging of nutrients will constitute a breakthrough for the characterization of nutrient transport 142
across root epithelia and will probably redefine existing models. Characterizing processes considered 143
to be well-known with a modern perspective can indeed lead to the identification of unsuspected 144
mechanisms. This was illustrated by recent efforts to identify the control mechanisms for formation 145
of the well-known Casparian strips through a multitude of forward and reverse genetic screens 146
[52,61–63,67,81,82]. The works, in addition to being of fundamental importance, identified a genetic 147
framework to transdifferentiate non-endodermal cells to form Casparian strips and provide a toolbox 148
to manipulate the epithelial properties of the root [83,84]. Knowledge transfer from these 149
fundamental approaches to crops will be particularly interesting in the coming years.
150 151
Acknowledgments 152
We apologize to authors whose relevant work on the radial transport of nutrients have not been 153
cited, either inadvertently or because of length constraints. We thank Lothar Kalmbach for critical 154
reading of the manuscript and Léa Jacquier, Linnka Legendre-Lefebvre and Vinay Shukla for feedback 155
on the figures.
156 157 158 159
Figure 1. Polarized transport across epithelia.
160
Schematic illustration of the functional likeliness between plant root (a,c) and the animal intestinal 161
gut epithelium (b,d). (a) Plant roots transport nutrients from the periphery (outside) to the 162
vasculature (inside) facilitated by root hairs and barred by diffusion barriers in the endodermis 163
(Casparian strips, in red; and suberin lamellae, in yellow). (b) The gut epithelium optimizes 164
acquisition of nutrients from the intestinal lumen (outside) to the blood vessels (inside) and are 165
marked by characteristic microvilli on apical surface, and tight junctions as a paracellular barrier 166
(red). (c) The outer-inner polarity in root epithelia with its three pathways for nutrient transport - 167
apoplastic (between cells, barred by Casparian strips), coupled transcellular (via polarized carriers 168
and barred by suberin) and symplastic (through plasmodesmata). (d) Apico-basolateral polarity of gut 169
epithelia with its two pathways for nutrient transport – paracellular (between cells controlled by 170
tight junction) and transcellular (via polarized carriers).
171 172
Figure 2. Polarized influx and efflux carriers in root layers.
173
Model of transcellular pathway in plant root through polarized influx and efflux carriers to the outer 174
and inner domains respectively. Schematic with examples from Arabidopsis with the pairs of boron 175
transporters NIP5;1 and BOR1/2 or BOR1 in the epidermis and endodermis, and the epidermal 176
nitrate and metal transporters NRT2.4 and IRT1.
177 178
References 179
*of special interest ** of outstanding interest 180
1. Doblas VG, Geldner N, Barberon M: The endodermis, a tightly controlled barrier for 181
nutrients. Curr Opin Plant Biol 2017, 39:136–143.
182
2. Dinneny JR: A gateway with a guard: How the endodermis regulates growth through 183
hormone signaling. Plant Sci 2014, 214:14–19.
184
3. Palmgren M: Plant epithelia: What is the role of the mortar in the wall? PLOS Biol 2018, 185
16:e3000073.
186
4. Che J, Yamaji N, Ma JF: Efficient and flexible uptake system for mineral elements in plants.
187
New Phytol 2018, 219:513–517.
188
5. Lodish HF: Molecular cell biology. W.H. Freeman; 2000.
189
6. Barberon M, Geldner N: Radial transport of nutrients: the plant root as a polarized 190
epithelium. Plant Physiol 2014, 166:528–37.
191
7. Geldner N: The Endodermis. Annu Rev Plant Biol 2013, 64:531–558.
192
8. Maizel A: Current Biology Dispatches Plant Biology: The Making of an Epithelium. 2018, 193
doi:10.1016/j.cub.2018.07.034.
194
9. Enstone DE, Peterson CA, Ma F: Root Endodermis and Exodermis: Structure, Function, and 195
Responses to the Environment. [date unknown], doi:10.1007/s00344-003-0002-2.
196
10. Ahn SJ, Shin R, Schachtman DP: Expression of KT/KUP Genes in Arabidopsis and the Role of 197
Root Hairs in K+ Uptake. PLANT Physiol 2004, 134:1135–1145.
198
11. Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G: Root hair systems biology. Trends Plant 199
Sci 2010, 15:641–650.
200
12. Høgh-Jensen H, Pedersen MB: Morphological Plasticity by Crop Plants and Their Potassium 201
Use Efficiency. J Plant Nutr 2003, 26:969–984.
202
13. Brown LK, George TS, Dupuy LX, White PJ: A conceptual model of root hair ideotypes for 203
future agricultural environments: what combination of traits should be targeted to cope 204
with limited P availability? Ann Bot 2013, 112:317–30.
205
14. Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS: Root hairs 206
improve root penetration, root–soil contact, and phosphorus acquisition in soils of different 207
strength. J Exp Bot 2013, 64:3711–3721.
208
15. Bates TR, Lynch JP: The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in 209
phosphorus acquisition. Am J Bot 2000, 87:964–70.
210
16. Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M: Characteristics of a 211
root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 2014, 212
65:1497–1512.
213
17. Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R: AtKC1, a 214
silent Arabidopsis potassium channel α-subunit modulates root hair K + influx. Proc Natl 215
Acad Sci 2002, 99:4079–4084.
216
18. Li S, Yu J, Zhu M, Zhao F, Luan S: Cadmium impairs ion homeostasis by altering K + and Ca 2+
217
channel activities in rice root hair cells. Plant Cell Environ 2012, 35:1998–2013.
218
19. Wang L, Guo M-Y, Thibaud J-B, Véry A-A, Sentenac H: A repertoire of cationic and anionic 219
conductances at the plasma membrane of Medicago truncatula root hairs. Plant J 2019, 220
doi:10.1111/tpj.14238.
221
20. Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R: K+ channel profile and 222
electrical properties of Arabidopsis root hairs. FEBS Lett 2001, 508:463–469.
223
21. Keyes SD, Daly KR, Gostling NJ, Jones DL, Talboys P, Pinzer BR, Boardman R, Sinclair I, 224
Marchant A, Roose T: High resolution synchrotron imaging of wheat root hairs growing in 225
soil and image based modelling of phosphate uptake. New Phytol 2013, 198:1023–1029.
226
22. Nakamura M, Grebe M: Outer, inner and planar polarity in the Arabidopsis root. Curr Opin 227
Plant Biol 2018, 41:46–53.
228
23. Salazar-Henao JE, Schmidt W: An Inventory of Nutrient-Responsive Genes in Arabidopsis 229
Root Hairs. Front Plant Sci 2016, 7:237.
230
24. Bates TR, Lynch JP: Stimulation of root hair elongation in Arabidopsis thaliana by low 231
phosphorus availability. Plant, Cell Environ 1996, 19:529–538.
232
25. Ma Z, Bielenberg DG, Brown KM, Lynch JP: Regulation of root hair density by phosphorus 233
availability in Arabidopsis thaliana. Plant, Cell Environ 2001, 24:459–467.
234
26. Müller M, Schmidt W: Environmentally induced plasticity of root hair development in 235
Arabidopsis. Plant Physiol 2004, 134:409–19.
236
27. Wei Yang TJ, Perry PJ, Ciani S, Pandian S, Schmidt W: Manganese deficiency alters the 237
patterning and development of root hairs in Arabidopsis. J Exp Bot 2008, 59:3453–3464.
238
28. Schmidt W, Schikora A: Different pathways are involved in phosphate and iron stress- 239
induced alterations of root epidermal cell development. Plant Physiol 2001, 125:2078–84.
240
29. Savage N, Yang TJW, Chen CY, Lin K-L, Monk NAM, Schmidt W: Positional signaling and 241
expression of ENHANCER OF TRY AND CPC1 are tuned to increase root hair density in 242
response to phosphate deficiency in Arabidopsis thaliana. PLoS One 2013, 8:e75452.
243
**30. Stanley CE, Shrivastava J, Brugman R, Heinzelmann E, van Swaay D, Grossmann G: Dual-flow- 244
RootChip reveals local adaptations of roots towards environmental asymmetry at the 245
physiological and genetic levels. New Phytol 2018, 217:1357–1369.
246
This paper presents an interesting microfluidics platform based tool that allows live imaging of 247
multiple Arabidopsis roots in parallel, in response to microalteration in the local root environment 248
using a perfusion system. This approach will be particularly valuable to study physiological responses 249
in the root given the advances in imaging tools, markers and reporters available in Arabidopsis.
250
31. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M: A 251
silicon transporter in rice. Nature 2006, 440:688–91.
252
32. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M: An efflux 253
transporter of silicon in rice. Nature 2007, 448:209–12.
254
33. Sasaki A, Yamaji N, Yokosho K, Ma JF: Nramp5 is a major transporter responsible for 255
manganese and cadmium uptake in rice. Plant Cell 2012, 24:2155–67.
256
34. Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y, Takemoto Y, Moriyama S, Che J, Moriyama Y, 257
Iwasaki K, et al.: A polarly localized transporter for efficient manganese uptake in rice. Nat 258
Plants 2015, 1:15170.
259
Fujiwara T: Arabidopsis boron transporter for xylem loading. Nature 2002, 420:337–340.
261
36. Alassimone J, Naseer S, Geldner N: A developmental framework for endodermal 262
differentiation and polarity. Proc Natl Acad Sci 2010, 107:5214–5219.
263
37. Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T: Polar 264
localization and degradation of Arabidopsis boron transporters through distinct trafficking 265
pathways. Proc Natl Acad Sci 2010, 107:5220–5225.
266
38. Miwa K, Wakuta S, Takada S, Ide K, Takano J, Naito S, Omori H, Matsunaga T, Fujiwara T: Roles 267
of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation 268
under boron limitation in Arabidopsis. Plant Physiol 2013, 163:1699–709.
269
39. Yoshinari A, Fujimoto M, Ueda T, Inada N, Naito S, Takano J: DRP1-Dependent Endocytosis is 270
Essential for Polar Localization and Boron-Induced Degradation of the Borate Transporter 271
BOR1 in Arabidopsis thaliana. Plant Cell Physiol 2016, 57:1985–2000.
272
40. Kiba T, Feria-Bourrellier A-B, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, 273
Miller A, Daniel-Vedele F, Sakakibara H, et al.: The Arabidopsis nitrate transporter NRT2.4 274
plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 2012, 24:245–
275
58.
276
41. Barberon M, Dubeaux G, Kolb C, Isono E, Zelazny E, Vert G: Polarization of IRON-REGULATED 277
TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis.
278
Proc Natl Acad Sci U S A 2014, 111:8293–8.
279
**42. Dubeaux G, Neveu J, Zelazny E, Vert G: Metal Sensing by the IRT1 Transporter-Receptor 280
Orchestrates Its Own Degradation and Plant Metal Nutrition. Mol Cell 2018, 69:953–964.e5.
281
The paper uncovers the function of the metal transporter IRT1 as a transceptor (transporter and 282
receptor), that directly senses excess of its non-iron metal substrates in the cytoplasm, to regulate its 283
own localization and degradation. This mechanism optimizes iron uptake relatively to other metals to 284
protect the plant from highly reactive and potentially toxic metals.
285
43. Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, Friml J, Vert G: Monoubiquitin- 286
dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron 287
uptake in plants. Proc Natl Acad Sci U S A 2011, 108:E450-8.
288
44. Kasai K, Takano J, Miwa K, Toyoda A, Fujiwara T: High boron-induced ubiquitination regulates 289
vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J Biol Chem 2011, 290
286:6175–83.
291
45. Wakuta S, Fujikawa T, Naito S, Takano J: Tolerance to Excess-Boron Conditions Acquired by 292
Stabilization of a BOR1 Variant with Weak Polarity in Arabidopsis. Front cell Dev Biol 2016, 293
4:4.
294
**46. Yoshinari A, Hosokawa T, Amano T, Beier MP, Kunieda T, Shimada T, Hara-Nishimura I, Naito 295
S, Takano J: Polar Localization of the Borate Exporter BOR1 Requires AP2-Dependent 296
Endocytosis. Plant Physiol 2019, doi:10.1104/pp.18.01017.
297
The study demonstrates the importance of the polarity in transport of boron shown by localization of 298
the borate exporter BOR1. The polar localization of BOR1 was shown to be maintained by AP2- 299
dependent endocytosis to support plant growth under low-B conditions, while the boron-induced 300
vacuolar sorting was found to be mediated through an AP2-independent endocytic pathway.
301
47. Yoshinari A, Takano J: Insights into the Mechanisms Underlying Boron Homeostasis in Plants.
302
Front Plant Sci 2017, 8:1951.
303
48. Cointry V, Vert G: The bifunctional transporter-receptor IRT1 at the heart of metal sensing 304
and signaling. New Phytol 2019, doi:10.1111/nph.15826.
305
**49. Wang S, Yoshinari A, Shimada T, Hara-Nishimura I, Mitani-Ueno N, Feng Ma J, Naito S, Takano 306
J: Polar Localization of the NIP5;1 Boric Acid Channel Is Maintained by Endocytosis and 307
Facilitates Boron Transport in Arabidopsis Roots. Plant Cell 2017, 29:824–842.
308
The paper shows the importance of polar localisation of NIP5;1 for efficient transport of boron in 309
roots. In the study, the N-terminal region of diffusion facilitator NIP5;1 is shown to be important for 310
the polar localization in the epidermal and endodermal cells maintained by clathrin mediated 311
endocytosis.
312
*50. Sotta N, Duncan S, Tanaka M, Sato T, Marée AF, Fujiwara T, Grieneisen VA: Rapid transporter 313
regulation prevents substrate flow traffic jams in boron transport. Elife 2017, 6.
314
The study provides an interesting insight into the dynamic transport systems that are coordinated 315
within a plant using regulation of boron transport as an example. With the help of a mathematical 316
modelling approach, they compare the transport across the root layers to study how the cells avoid 317
the internal roadblock in boron transport. They found rapid changes in the number of transporter 318
proteins on the root surface to be the mechanism plants need to maintain a steady supply of boron.
319
51. Caspary R: Remarks on the protective sheath and the formation of stem and root 320
(translated from German). Jahrbücher für wissenschaftliche Bot 1865, 4:101–124.
321
*52. Alassimone J, Fujita S, Doblas VG, van Dop M, Barberon M, Kalmbach L, Vermeer JEM, Rojas- 322
Murcia N, Santuari L, Hardtke CS, et al.: Polarly localized kinase SGN1 is required for 323
Casparian strip integrity and positioning. Nat plants 2016, 2:16113.
324
The study shows polar localization of SCHENGEN1 (SGN1), a receptor-like cytoplasmic kinase 325
localized to the outer endodermal plasma membrane. It is required for the positioning and correct 326
formation of the centrally located CASPARIAN STRIP ASSOCIATED PROTEIN (CASP) domain in the 327
endodermis. The paper describes a neat screen to identify Casparian strip defective mutants and a 328
fine combination of genetic analyses and subcellular structure studies to understand Casparian strip 329
formation.
330
53. Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N: Casparian strip diffusion barrier 331
in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci 2012, 332
109:10101–10106.
333
54. Barbosa ICR, Rojas-Murcia N, Geldner N: The Casparian strip—one ring to bring cell biology 334
to lignification? Curr Opin Biotechnol 2019, 56:121–129.
335
**55. Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath 336
C, Takano J, Salt DE, et al.: Adaptation of Root Function by Nutrient-Induced Plasticity of 337
Endodermal Differentiation. Cell 2016, 164:447–59.
338
The paper provides key evidence on the ability of the root to synthesize and degrade suberin in 339
response to a wide range of nutrient stresses, mediated by the stress hormones abscisic acid and 340
ethylene. It highlights the function of suberin as a transcellular barrier for diffusion of nutrients 341
through plasma membrane.
342
*56. Andersen TG, Naseer S, Ursache R, Wybouw B, Smet W, De Rybel B, Vermeer JEM, Geldner N:
343
Diffusible repression of cytokinin signalling produces endodermal symmetry and passage 344
cells. Nature 2018, 555:529–533.
345
Study presents a framework for passage cell differentiation with a non-cell-autonomous repression 346
endodermal cells that are less cytokinin-ABA-sensitive and more cytokinin-ABA-sensitive 348
respectively.
349
57. Peterson CA, Enstone DE: Functions of passage cells in the endodermis and exodermis of 350
roots. Physiol Plant 1996, 97:592–598.
351
58. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y:
352
Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate 353
loading to the xylem. Plant Cell 2002, 14:889–902.
354
**59. Duan F, Giehl RFH, Geldner N, Salt DE, von Wirén N: Root zone–specific localization of AMTs 355
determines ammonium transport pathways and nitrogen allocation to shoots. PLOS Biol 356
2018, 16:e2006024.
357
The study shows symplastic transport being more efficient under low external ammonium supply.
358
Suberization of endodermal cells leads to shift in the expression of ammonium transporters to the 359
cortical cells. The work point to an interesting synergism between apoplastic and symplastic 360
transport along the root axis and its contribution to the partitioning of ammonia between roots and 361
shoots.
362
60. Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot M Lou, Salt DE: Dirigent 363
domain-containing protein is part of the machinery required for formation of the lignin- 364
based Casparian strip in the root. Proc Natl Acad Sci U S A 2013, 110:14498–503.
365
61. Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer JEM, Yamazaki M, Li G, 366
Maurel C, Takano J, et al.: A receptor-like kinase mutant with absent endodermal diffusion 367
barrier displays selective nutrient homeostasis defects. Elife 2014, 3:e03115.
368
62. Kamiya T, Borghi M, Wang P, Danku JMC, Kalmbach L, Hosmani PS, Naseer S, Fujiwara T, 369
Geldner N, Salt DE: The MYB36 transcription factor orchestrates Casparian strip formation.
370
Proc Natl Acad Sci U S A 2015, 112:10533–8.
371
**63. Li B, Kamiya T, Kalmbach L, Yamagami M, Yamaguchi K, Shigenobu S, Sawa S, Danku JMC, Salt 372
DE, Geldner N, et al.: Role of LOTR1 in Nutrient Transport through Organization of Spatial 373
Distribution of Root Endodermal Barriers. Curr Biol 2017, 27:758–765.
374
The study identifies the gene LOTR1 being essential for Casparian strip formation. lotr1 mutants 375
display disrupted Casparian strips, ectopic suberization of endodermal cells, and lower accumulation 376
of shoot calcium. Expression of suberin degrading enzyme in the endodermis of the mutant led to 377
ectopic suberization and reduced calcium transport to the stele and translocation to the shoots in 378
this mutant.
379
64. Wang P, Calvo-Polanco M, Reyt G, Barberon M, Champeyroux C, Santoni V, Maurel C, Franke 380
RB, Ljung K, Novak O, et al.: Surveillance of cell wall diffusion barrier integrity modulates 381
water and solute transport in plants. Sci Rep 2019, 9:4227.
382
65. Barberon M: The endodermis as a checkpoint for nutrients. New Phytol 2017, 213:1604–
383
1610.
384
66. Persson DP, Chen A, Aarts MGM, Salt DE, Schjoerring JK, Husted S: Multi-Element Bioimaging 385
of Arabidopsis thaliana Roots. Plant Physiol 2016, 172:835–847.
386
67. Kalmbach L, Hématy K, De Bellis D, Barberon M, Fujita S, Ursache R, Daraspe J, Geldner N:
387
Transient cell-specific EXO70A1 activity in the CASP domain and Casparian strip localization.
388
Nat Plants 2017, 3.
389
*68. Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, Belkhadir 390
Y, Geldner N: Root diffusion barrier control by a vasculature-derived peptide binding to the 391
SGN3 receptor. Science 2017, 355:280–284.
392
The study identifies two stele-expressed peptides (CASPARIAN STRIP INTEGRITY FACTORS, CIF1/2) 393
that bind to receptor-like kinase SCHENGEN3/GASSHO1 (SGN3/GSO1). The CIF1/2-SGN3 considered 394
to be a part of a barrier surveillance system to ensure effective sealing of the Casparian strip network 395
with defects in the system leading to ectopic lignin and suberin in the endodermis.
396
*69. Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y: A peptide 397
hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots.
398
Science 2017, 355:284–286.
399
Two stele-expressed peptides Casparian strip Integrity Factor 1 (CIF1) and CIF2 were found to bind 400
specifically to the endodermal leucine-rich repeat receptor kinase GASSHO1 (GSO1)/SCHENGEN3 and 401
its homolog GSO2 and important for the formation and maintenance of a functional Casparian strip.
402
70. Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Schreiber L, Mathew MK: The role of 403
root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 2009, 404
230:119–34.
405
71. Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK: Root apoplastic barriers 406
block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 2011, 62:4215–4228.
407
72. Shiono K, Ando M, Nishiuchi S, Takahashi H, Watanabe K, Nakamura M, Matsuo Y, Yasuno N, 408
Yamanouchi U, Fujimoto M, et al.: RCN1/OsABCG5, an ATP-binding cassette (ABC) 409
transporter, is required for hypodermal suberization of roots in rice ( Oryza sativa ). Plant J 410
2014, 80:40–51.
411
73. Líška D, Martinka M, Kohanová J, Lux A: Asymmetrical development of root endodermis and 412
exodermis in reaction to abiotic stresses. Ann Bot 2016, 118:667–674.
413
74. Ranathunge K, Schreiber L, Bi Y-M, Rothstein SJ: Ammonium-induced architectural and 414
anatomical changes with altered suberin and lignin levels significantly change water and 415
solute permeabilities of rice (Oryza sativa L.) roots. Planta 2016, 243:231–49.
416
75. Champeyroux C, Bellati J, Barberon M, Rofidal V, Maurel C, Santoni V: Regulation of a plant 417
aquaporin by a Casparian strip membrane domain protein-like. Plant Cell Environ 2019, 418
doi:10.1111/pce.13537.
419
76. Carter KP, Young AM, Palmer AE: Fluorescent sensors for measuring metal ions in living 420
systems. Chem Rev 2014, 114:4564–601.
421
77. Kopittke PM, Punshon T, Paterson DJ, Tappero R V, Wang P, Blamey FPC, van der Ent A, Lombi 422
E: Synchrotron-Based X-Ray Fluorescence Microscopy as a Technique for Imaging of 423
Elements in Plants. Plant Physiol 2018, 178:507–523.
424
78. Moore KL, Chen Y, van de Meene AML, Hughes L, Liu W, Geraki T, Mosselmans F, McGrath SP, 425
Grovenor C, Zhao F-J: Combined NanoSIMS and synchrotron X-ray fluorescence reveal 426
distinct cellular and subcellular distribution patterns of trace elements in rice tissues. New 427
Phytol 2014, 201:104–115.
428
79. Ondrasek G, Rengel Z, Clode PL, Kilburn MR, Guagliardo P, Romic D: Zinc and cadmium 429
mapping by NanoSIMS within the root apex after short-term exposure to metal 430
contamination. Ecotoxicol Environ Saf 2019, 171:571–578.
431
80. Nakanishi TM: What you can see by developing real-time radioisotope imaging system for 432
1695.
434
81. Roppolo D, De Rybel B, Tendon VD, Pfister A, Alassimone J, Vermeer JEM, Yamazaki M, 435
Stierhof Y-D, Beeckman T, Geldner N: A novel protein family mediates Casparian strip 436
formation in the endodermis. Nature 2011, 473:380–383.
437
82. Liberman LM, Sparks EE, Moreno-Risueno MA, Petricka JJ, Benfey PN: MYB36 regulates the 438
transition from proliferation to differentiation in the Arabidopsis root. Proc Natl Acad Sci U S 439
A 2015, 112:12099–104.
440
*83. Drapek C, Sparks EE, Marhavy P, Taylor I, Andersen TG, Hennacy JH, Geldner N, Benfey PN:
441
Minimum requirements for changing and maintaining endodermis cell identity in the 442
Arabidopsis root. Nat Plants 2018, 4:586–595.
443
The study shows transcription factors SHORTROOT and MYB36 by themselves being insufficient to 444
induce ectopic endodermal features and introduces the role of a stele derived signaling peptide CIF2 445
to establish endodermal identity. It highlights the basic machinery required to establish endodermal 446
identity to non-native cell types.
447
*84. Li P, Yu Q, Gu X, Xu C, Qi S, Wang H, Zhong F, Baskin TI, Rahman A, Wu S: Construction of a 448
Functional Casparian Strip in Non-endodermal Lineages Is Orchestrated by Two Parallel 449
Signaling Systems in Arabidopsis thaliana. Curr Biol 2018, 28:2777–2786.e2.
450
The study proposes a model in which SHORTROOT (SHR) on one hand activates MYB36 signalling that 451
regulates CASP1 expression and lignin polymerization while in parallel, it activates SCARECROW and 452
SCHENGEN3 (SGN3) for correct placement of the strip. Interestingly, the SHR-CIF combination was 453
suggested to be sufficient to introduce ectopic Casparian strip formation in the root.
454
Microvilli
Apical membrane Tight junction (paracellular barrier)
Basolateral membrane Capillary
Paracellular
transport Transcellular transport Root hair cell
Non-hair cell
Passage cell Plasmodesmata
Cortex
Endodermis Pericycle
Apoplastic pathway
Transcellular pathway Symplastic
pathway
Suberin lamellae (transcellular barrier)
Casparian strip (apoplastic barrier)
Phloem
Outer apoplast Inner apoplast Xylem
Figure 1
b a
d c
Outside
Inside Outside
Inside
Outer membrane Inner membrane Epidermis
Influx carriers NIP5;1NRT2,4IRT1
Efflux carriers BOR1BOR2 ? ?
Influx carriers NIP5;1
Efflux carriers BOR1
Transcellular pathway Figure 2
Influx carriers
Efflux carriers
epidermis (trichoblast)
cortex
endodermis
