# Integrating membrane transport, signaling, and physiology

Yi-Fang Tsay, Michael Blatt, Matthew Gilliham, Christophe Maurel, Nicolaus von Wirén

► To cite this version:

Yi-Fang Tsay, Michael Blatt, Matthew Gilliham, Christophe Maurel, Nicolaus von Wirén. Integrating membrane transport, signaling, and physiology. Plant Physiology, 2022, 188 (2), pp.921-923. 10.1093/plphys/kiab585. hal-03655511

HAL Id: hal-03655511

https://hal.inrae.fr/hal-03655511

Submitted on 28 Nov 2022

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
Integrating membrane transport, signaling and physiology

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

1. Institute of Molecular Biology, Academia Sinica, Taipei 11529, Taiwan;
   yftsay@gate.sinica.edu.tw

2. Laboratory of Plant Physiology and Biophysics, Bower Building, University of
Glasgow, Glasgow G12 8QQ, UK

3. ARC Centre of Excellence in Plant Energy Biology, Waite Research Institute & School of Agriculture Food and Wine, University of Adelaide, PMB1, Glen Osmond, SA 5064, Australia

4. BPMP, University Montpellier, CNRS, INRAE, Institute Agro, Montpellier, France

5. Molecular Plant Nutrition, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Stadt Seeland, OT Gatersleben, Germany

Membranes constitute a barrier that compartmentalizes cells and organelles from their surrounding environment. Transport across these barriers, mediated in the most part by channels, transporters and pumps, is essential for many aspects of cellular function. In plants, approximately 7% of the encoded proteins host at least four transmembrane spans and are potentially involved in membrane transport. Membrane transport plays key roles in including nutrition, cellular homeostasis, signaling and development, and is a vital component of responses to biotic and abiotic stresses. This Focus Issue brings together updates and research articles that address some of most exciting and recent advances in our understanding of the molecular mechanisms underlying membrane transport, its integration with signaling, and its roles in homeostasis. Here, we highlight the contents of the 14 Updates presented in this Focus Issue.

Transport integration in signal generation and plant development

Plants have evolved many more ATP-binding cassette transporters (ABC) than other organisms. Youngsook Lee's group, that has worked on ABC transporters for more than two decades, comprehensively summarizes the recent developments on ABC transporters, including newly identified functions and regulatory mechanisms (Do et al, 2021). The Update outlines those transport functions that have been deciphered using physiological data and those which have been verified by functional assays in heterologous cell systems. The authors discuss a number of
40

41

42

43

44

45

46

47

48

49

50

51

52

53

54

55

56

57

58

59

60

61

62

63

64

65

66

67

68

69

70

71

72

73

74

75

76

77

78

79

outstanding questions such as how ABC transporters play such diverse roles in plants and why so many ABC transporter genes have been retained in plant genome.

Metalloids are mineral elements that are often widely present in soils. In their update, Yamaji and Ma (2021) focus on Boron (B), Silicon (Si) and Arsenic (As), covering the range of metalloids relevant to plants, whether essential, beneficial, or biotoxic. These three metalloids share overlapping transport pathways for uptake and distribution throughout plants. Central to these pathways is the metalloid influx mediated by highly specialized aquaporins of the NIP subfamily. The NIPs operate with specific efflux transporters displaying distinct polar localizations. Understanding the mechanisms by which substrate specificity of these localizations is determined and their functional divergence among tissues or even plant species (monocots vs. dicots) will provide novel insights into the molecular physiology of metalloids in plants.

γ-aminobutyric acid (GABA) is a key signaling molecule in animals, but less is known about the roles and actions of GABA in plants. Xu, Sai and Gilliham (2021) update us on the physiological impact of GABA in plants summarizing the current evidence for the roles of aluminum-activated malate transporters (ALMTs) being the targets of GABA signaling in guard cells to regulate water use efficiency, as well as in pollen to regulate fertility. They speculate on other potential targets of GABA in plants, such as H⁺-ATPase, potassium channels, and 14-3-3 proteins. They also discuss the link of GABA to glutamate and hormones, as well as the potential role of GABA for long-distance signaling.

Cellular phosphate (Pi) homeostasis is regulated by inositol pyrophosphates (PP-InsP), which act as intracellular messengers and are perceived by the SPX domains of various proteins involved in Pi transport and signaling. In their Update, Wang et al. (2021) explore the dynamics of Pi and PP-InsP metabolism. They describe the role of PP-InsP as ligands to modulate the interactions between SPX proteins and transcriptional activators in the phosphate starvation response, thereby ultimately coordinating cross-membrane Pi transport and cellular Pi homeostasis.

Integrating Transport within and between cellular membranes

Membrane nanodomains are defined as submicron protein and/or lipid assemblies, whose structural characterization has greatly profited from recent advances in microscopy techniques. The Update by Martinière and Zelazny (2021) illustrates the role of membrane nano-organization in regulating of molecule
80

81

82

83

84

85

86

87

88

89

90

91

92

93

94

95

96

97

98

99

100

101

102

103

104

105

106

107

transport in plants. They focus on plasma membrane nanodomain formation, which arises from functional assembly of sterols, sphingolipids, and specific proteins, thereby regulating internalization of transporters in response to stimuli or effecting co-clustering of proteins with their regulators.

The Update from Mehlhorn, Asseck and Grefen (2021) sets out the background to our understanding of protein maturation and insertion into the lipid bilayers with a particular emphasis on tail-anchored proteins. As they note, the textbook models of protein insertion mechanisms lack credibility for those secretory or membrane proteins which lack an amino-terminal signal sequence or transmembrane domain. They review our current state of knowledge about tail-anchored proteins, harboring a single carboxy-terminal transmembrane domain, and they address potential alternative, post-translational insertion routes into the endoplasmic reticulum membrane.

In recent years, the technologies for exploring the subcellular mechanics of Ca²⁺ signaling have greatly expanded with sensors that can be targeted to specific locations within a plant cell. Two Updates in this Focus Issue evaluate these tools and the information that they yield. The review by He et al (2021) examines transporters likely to be involved in Ca²⁺ signal transmission, as well as those of another divalent (Mn²⁺), their transport across membranes, and their notable association with glutamate receptor-like proteins (GLRs) and several linked pumps and coupled transporters. Taking an organelle-focused perspective of the interactive mechanics behind Ca²⁺ signaling, Resentini et al. (2021) address questions about how unique characteristics of these signals may have arisen and how the divalent ions are resequestered. They include examples of how latencies in stomatal responsiveness to light and CO₂ have evolved (Jezek et al 2021), as well as temporal properties of Ca²⁺ oscillations.

Finally, Tomkins, Hughes and Morris (2021) revisit the fundamentals of ion and solute diffusion, emphasizing on the physics of passive transport systems and the driving forces that give rise to diffusive and bulk flow processes in and out of cells.

108

109

110

111

112

113

## Transport integration in environmental interactions

114

115

116

117

118

119

Kv (potassium voltage) channels in plants are important for nutrition by mediating potassium uptake from the soil and distribute it through the whole plant, and also for stomata movements. The Update review by Lefoulon (2021) focuses on how Kv channels work with an emphasis on their mechanistics, our knowledge of plant Kv channel structure, and the structures of closely-related channels in other
120 organisms. Lefoulon (2021) addresses issues from the selectivity of the Kv channels
to their gating by voltage, and finally how auxiliary proteins can regulate their
function in the face of environmental stress and how the gating properties may be
manipulated to affect plant growth and physiology.
124

125 Plasma membrane H⁺-ATPases and Ca²⁺-ATPases are autoregulated by
cytoplasmic concentrations of H⁺ and Ca²⁺, respectively, to generate steep gradients
across membranes as a prerequisite for substrate transport and cellular signaling.
126
127 The Update by Fuglsang and Palmgren (2021) highlights the role of phosphorylated
128 sites in the terminal regulatory domains of these pumps. Although some of these
129 phosphosites appear to be constantly phosphorylated and may function as major
130 switches, others appear to be dynamically phosphorylated to enable gradual
131 reductions in their activity.
132

133
134 Kim et al. update us on transport processes, in which sugars and amino acids
135 are secreted from plant cells by SWEET-type and UmamiT-type exporters,
136 respectively. Supported by instructive illustrations, key aspects relate to their cell
137 type-specific expression in phloem parenchyma and companion cells to govern the
138 distribution of assimilates in plants, as well as to their function in roots and other
139 organs to feed beneficial or pathogenic microbes.
140

141 Apart from their fascinating and unique biology, carnivorous plants have
142 been highly relevant model systems for exploring long distance electrical signaling
143 in plants, since the early work of Charles Darwin. Böhm and Scherzer (2021) review
144 this topic, including their own research on signaling events in Venus flytrap
145 (Dionaea muscipula L.) and results from other research groups. The ion channel
146 activities underliying action potentials, their interaction with calcium and links to
147 downstream jasmonate signaling now provide a strong framework for
148 understanding the trap closure mechanism. Many other processes related to trap
149 biomechanics and the respective roles of growth and membrane transport during
150 slow trap reopening remain exciting topics for future research.
151

152 Plants sense the concentration of the major photosynthetic substrate CO2
153 within their leaves and, consequently, alter atmospheric connectivity by opening or
154 closing their stomatal pores. Dubeaux et al. (2021) update a current understanding
155 of how plants sense and respond to changing levels of CO2, focusing on signaling
156 mechanisms that are known or might be involved in stomatal aperture responses to
157 low or high CO2 concentrations. They also include a brief topical perspective on the
158 effects of rising atmospheric CO2 concentrations in terms of stomatal densities and
159 their potential impact on crop productivity.
160
160

161

162

163

164

165

166

167

168

169

170

171

172

173

174

175

176

177

178

179

180

181

182

Water may constitute up to 98% of the weight of fully turgid plant tissues. Cross-membrane water transport mediated by aquaporins is critical to plant expansion/growth, dehydration and germination of pollen and seeds, stomatal closure etc. Accordingly, aquaporins represent central membrane targets of diverse environmental and intrinsic signals. Maurel et al (2021) update us on how aquaporins are regulated by drought, salinity, cold, nutrients, hormones, and other biotic factors to maintain the plant water status. Interestingly, the multiple results on the role of aquaporins in stomatal movement are discussed with explanations proposed: due to their H₂O₂ transport activity, guard cell aquaporins function both as players and targets of ABA and flagellin signalling during stomatal closure.

The combined and considerable efforts of the editorial team over two years have culminated in this Focus Issue. We hope you enjoy reading it as much as we have enjoyed assembling it. Much of the contents of this Focus Issue arise from the open discussions and interactions that took place at the 18th International Workshop in Plant Membrane Biology, in Glasgow in 2019. This Focus Issue serves as a bridge leading you to the next International Workshop in Plant Membrane Biology, scheduled for October 17-21 of 2022 in Taiwan, where all of the latest advances in the above areas will be showcased. If nothing else, these Updates and the Workshop show how rapidly the field is now evolving.
## Parsed Citations

Böhm J, Scherzer S (2021) Signaling and transport processes related to the carnivorous lifestyle of plants living on nutrient-poor soil. Plant Physiol 187: 2017-2031

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Do THT, Martinioa E, Lee Y, Hwang JU (2021) 2021 update on ATP-binding cassette (ABC) transporters: how they meet the needs of plants. Plant Physiol 187: 1876-1892

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Dubeaux G, Hsu PK, Ceciliato PHO, Swink KJ, Rappel WJ, Schroeder JI (2021) Deep dive into CO2-dependent molecular mechanisms driving stomatal responses in plants. Plant Physiol 187: 2032-2042

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Fuglsang AT and Palmgren M (2021) Proton and calcium pumping P-type ATPases and their regulation of plant responses to the environment. Plant Physiol 187: 1856-1875

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

He J, Rössner N, Minh Hoang TT, Alejandro S, Peiter E (2021) Transport, functions, and interaction of calcium and manganese in plant organellar compartments. Plant Physiol 187: 1940-1972

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Jezek M, Silva-Alvim FAL, Hills A, Donald N, Ishka MR, Shadbolt J, He B, Lawson T, Harper JF, Wang Y, Lew VL, Blatt MR (2021) Guard cell endomembrane Ca2+-ATPases underpin a 'carbon memory' of photosynthetic assimilation that impacts on water use efficiency. Nature Plants 7,1301-7

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Kim JY, Loo EPI, Pang TY, Lercher M, Frommer WB, Wudick MM (2021) Cellular export of sugars and amino acids: role in feeding other cells and organisms. Plant Physiol 187: 1893-1915

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Lefoulon C (2021) The bare necessities of plant K+ channel regulation. Plant Physiol 187: 2092-2109

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Martinière A, Zelazny E (2021) Membrane nanodomains and transport functions in plant. Plant Physiol 187: 1839-1855

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Maurel C, Tournaire-Roux C, Verdoucq L, Santoni V (2021) Hormonal and environmental signaling pathways target membrane water transport. Plant Physiol 187: 2056-2070

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Mehlhorn D, Asseck LY, Grefen C. (2021) Looking for a safe haven: tail-anchored proteins and their membrane insertion pathways. Plant Physiol 187: 1916-1928

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Resentini F, Ruberti C, Grenzi M, Bonza MC, Costa A (2021) The signatures of organellar calcium. Plant Physiol 187: 1985-2004

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Tomkins M, Hughes N, Morris RJ (2021) An update on passive transport in and out of plant cells. Plant Physiol 187: 1973-1984

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Wang Z, Kuo HF, Chiou TJ (2021) Intracellular phosphate sensing and regulation of phosphate transport systems in plants. Plant Physiol 187: 2043-2055

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Xu B, Sai N, Gilliham M (2021) The emerging role of GABA as a transport regulator and physiological signal. Plant Physiol 187: 2005-2016

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)

Yamaji N, Ma JF (2021) Metalloid transporters and their regulation in plants. Plant Physiol 187: 1929-1939

Google Scholar: [Author Only](#) [Title Only](#) [Author and Title](#)