understanding the functions and mechanisms of plant...

Understanding the functions and mechanisms of plantcytoskeleton in response to environmental signalsXiangfeng Wang and Tonglin Mao

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Plants perceive multiple physiological and environmental

signals in order to fine-tune their growth and development. The

highly dynamic plant cytoskeleton, including actin and

microtubule networks, can rapidly alter their organization,

stability and dynamics in response to internal and external

stimuli, which is considered vital for plant growth and

adaptation to the environment. The cytoskeleton-associated

proteins have been shown to be key regulatory molecules in

mediating cytoskeleton reorganization in response to multiple

environmental signals, such as light, salt, drought and biotic

stimuli. Recent findings, including our studies, have expanded

knowledge about the functions and underlying mechanisms of

the plant cytoskeleton in environmental adaptation.

Address

State Key Laboratory of Plant Physiology and Biochemistry, Department

of Plant Sciences, College of Biological Sciences, China Agricultural

University, Beijing 100193, China

Corresponding author: Mao, Tonglin ([email protected])

Current Opinion in Plant Biology 2019, 52:86–96

This review comes from a themed issue on Cell biology

Edited by Eva Benkova and Yasin Dagdas

https://doi.org/10.1016/j.pbi.2019.08.002

1369-5266/ã 2019 Elsevier Ltd. All rights reserved.

IntroductionThe plant cytoskeleton is composed of actin and micro-

tubule (MT) networks. The MTs are polymerized by the

a-tubulin and b-tubulin heterodimers and actin filaments

(F-actin) are polymerized by G-actin. Both MTs and

F-actin are filamentous structures with similar properties;

however, their organization, dynamics and cellular roles

are varied [1–4]. The treadmilling model has been used to

describe the dynamics of both structures, suggesting the

balanced polymerization at the plus (barbed) end and

depolymerization at the minus (pointed) end through a

single MT and actin filament [5–7]. In addition, both

cytoskeletal structures have their unique features. The

dynamic instability of MTs has been long described

showing that growing and shrinking MTs co-exist and

the individual MT could transit between two states

through catastrophe and rescue events, which is crucial


for the fast reorganization of the MT arrays [8]. Multiple

MAPs (MT-associated proteins) and other regulators,

including g-tubulin complex (g-TuC), bundling proteins,

plus-end-tracking proteins, severing proteins, and

destabilizing proteins, choreograph the dynamics and

organization of MTs [8–10]. For the actin cytoskeleton,

a stochastic dynamic model is recently proposed to show

that severing is the major event contributing to the actin

turnover instead of depolymerization [6]. The dynamic

activities of actin filaments are complex and tightly regu-

lated by multiple ABPs (actin-binding proteins), includ-

ing nucleation factors, barbed-end capping proteins,

severing factors, and bundling proteins [1,6]. In addition,

it has been reported that the actin cytoskeleton could

interact with different membranes through specific pro-

teins, which is essential for its major cellular roles includ-

ing vesicle delivery, organelle movement and driving the

membrane bending [6,11,12]. In particular, an emerging

role of plant MTs in SNX1 (sorting nexin 1) endosome

tethering has also been supported by recent findings,

showing the complexity of cytoskeleton-membrane

interaction [12,13].

The organization and dynamics of the plant cytoskeleton

change in response to diverse developmental cues and

external signals, such as light, cold and mechanical stress,

thus participating in plant adaptation to the environment

[14,15�,16–22]. In recent decades, many MAPs and ABPs

have been characterized and identified as indispensable to

sense the environmental signals and regulate the signal-

induced cytoskeleton reorganization [15�,16,23–25]. In this

review, we highlight recent advances regarding the role of

the plant cytoskeleton in plant environmental adaptation,

and the key molecules regulating cytoskeleton remodeling

in response to specific environmental signals, including

light, salt,droughtandbiotic stimuli.Finally,wediscuss the

little understood but important gaps between upstream

signals and the cytoskeleton, as well as the exact functions

of cytoskeleton remodeling in cellular processes.

Roles and mechanisms of the cytoskeleton inresponse to light signalsMTs in light response

Light is not only essential for photosynthesis but is one of

the major environmental cues during plant growth and

development. In darkness, etiolated seedlings exhibit a

rapidly elongating hypocotyl, small unopened cotyledons

on an apical hook and a short primary root [26,27]. When

emerged from soil, seedlings perceive light signals and

undergo photomorphogenesis such as termination of

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Cytoskeleton and its role in environmental adaptation Wang and Mao 87

hypocotyl elongation [28–30]. It is well established that

the status of plant cell growth is closely related to the

orientation of cortical MTs, which in turn alters the

orientation of newly deposited cellulose microfibrils

and regulates the direction of cell expansion [2–4]. In

rapidly elongating hypocotyl cells, the parallel arrays of

cortical MTs are predominantly transversely oriented to

the hypocotyl longitudinal growth axis, and they exhibit

predominantly oblique or longitudinal directions once the

accelerative phase of cell elongation slows [31,32]. It has

been observed for decades that the reorganization of

cortical MT arrays is induced to guide cellulose deposi-

tion and suppress hypocotyl cell elongation when etio-

lated plants are exposed to light [32,33]. Moreover,

MT-severing protein katanin creates new MT ends at

crossovers and amplifies the longitudinal arrays at high

angles, driving the blue light-induced 90� reorientation of

cortical MT transverse arrays within 15 min in hypocotyl

epidermal cells [34��,35]. The conserved +TIP CLASP

(cytoplasmic linker-associated protein) was later shown to

stabilize the newly generated plus ends [36�]. Impor-

tantly, this severing-based MT reorientation requires

blue-light photoreceptor phototropins, indicating the

molecular linkage between light-induced MT reorienta-

tion and light signaling [34��]. Another major means of

generating new MT, nucleation from g-tubulin com-

plexes, was reported to be regulated by the B00 subunitof the PP2A phosphatase TON2 (TONNEAU2)/FASS,

which is required for light-induced MT array reorganiza-

tion by altering the ratio of branching to parallel

MT-bound nucleation. However, whether and how

TON2 activity on MT nucleation is regulated by light

signaling remains unclear [37].

Some other MAPs have been identified as involved in MT

reorganization in response to light, and how they are regu-

lated by light signals has been elucidated. Li et al. showed

that light stimulated the increase of calcium level in hypo-

cotyl cells, which in turn dissociated the MT-destabilized

protein MDP25 from the plasma membrane (PM) into

cytosol [38]. Then MDP25 mediated the cortical MT reor-

ganization from transverse to oblique and longitudinal arrays

in favor of light-inhibited hypocotyl cell elongation when

Arabidopsis seedlings were transferred from darkness to light

[38]. The MAP WDL3 is a negative regulator of hypocotyl

elongation and is degraded by the 26S proteasome in dark-

ness. When etiolated seedlings were transferred to the light,

WDL3 protein was stabilized and modulated cortical MT

reorganization [39]. Furthermore, Lian et al. found that

COP1 (CONSTITUTIVE PHOTOMORPHOGENIC

1), an E3 ubiquitin ligase acting as a central repressor of

seedling photomorphogenesis, directly targets and degrades

WDL3 in darkness, revealing a novel mechanism that light

signaling induces cortical MT reorganization through

directly regulating MAP protein level [40��]. Generally,

cellular relocalization and ubiquitin modification are rela-

tively quick regulatory processes, which is in agreement with


the phenomenon of rapid MT reorientation induced by

light. Interestingly, some MAPs express specifically in dark-

ness or in light and are involved in cell elongation, such as

SPR1 (SPIRAL1) and MDP60 [41,42]. How these MAPs are

regulated and whether they participate in light signaling-

induced cortical MT reorganization are worthy of future

investigation. We present a model for the current under-

standing of the regulation of light-induced cortical MT

reorientation in Figure 1.

F-actin in light response

In plant cells, a characteristic cellular process in response

to light is the movement of chloroplasts, which exhibit

avoidance response to strong light, and accumulation

response to weak light [23,43,44]. A kind of specialized

short actin filaments observed along the chloroplast

periphery and termed cp-actin (chloroplast-actin) fila-

ments are believed to mediate chloroplast photoreloca-

tion and anchoring to the PM [23]. The actin-driven

chloroplast directional movement has been discussed in

several reviews [23,44,45]. Here we highlight several key

factors. CHUP1 (chloroplast unusual positioning1) is a

plant-specific ABP localized on the chloroplast envelope.

In the chup1 mutant, cp-actin filaments are lacking, and

the chloroplasts showed aggregation clusters and did not

move in response to blue light irradiation, supporting the

important function of CHUP1 in polymerizing cp-actin

filaments [46,47]. Another ABP THRUMIN1 with actin-

bundling activity localizes to the PM and its actin locali-

zation is light-dependent and phototropin-dependent,

making it an important link between light perception

and the dynamic of actin filaments [48,49]. Two KAC

(KINESIN-LIKE PROTEIN FOR ACTIN-BASED

CHLOROPLAST MOVEMENT) proteins were also

identified to mediate chloroplast anchoring to the PM

and actin-based chloroplast movement [50,51].

Roles and mechanisms of the cytoskeleton inplant response to salt stressMTs in salt response

High soil salinity significantly affects crop growth and

yield. Evidences have demonstrated that regulation of

cortical MTs is crucial for plant adaptation to salt stress

[24,52,53��]. Decreased levels of a-tubulin and b-tubulinin the pfd3 and pfd5 (i.e. prefoldin subunits 3 and 5)

mutants, resulted in seedlings hypersensitive to high salt

treatment [54]. The a-tubulin is phosphorylated by a

mitogen-activated protein kinase phosphatase PHS1

(PROPYZAMIDE-HYPERSENSITIVE 1), which gen-

erates a polymerization-incompetent tubulin isoform and

thereby promotes MT depolymerization under salt stress

[55��,56]. Moreover, Wang et al. reported that prolonged

exposure to salt treatment induces cortical MT reorgani-

zation, including fast depolymerization and reassembly of

new MT networks [53��]. Particularly, this physiological

process is considered to be vital for seedling survival

under salt stress and provides the cornerstone for further


88 Cell biology

Figure 1

Light

Dark

growth axis

Ca2+

Tubulin heterodimer

COP1(E3) E226Sproteosome

MDP25

Katanin complex

KTN80 KTN1

WDL3

TON2

CLASP

γ-TURC

WT

Blue light

ton2 mutant

Current Opinion in Plant Biology

Schematic model of MT-mediated plant cell elongation in response to light signal. Multiple MAPs are involved in regulating the process. (1) The

MT-destabilized protein MDP25 dissociates from the PM when cytoplasmic Ca2+ increases in response to light, and then binds and reorganizes

the cortical MTs from transverse to oblique and longitudinal arrays. (2) In darkness, WDL3 is ubiquitinated by COP1 E3 ligase and degraded by

26S proteasome. (3) When plants are transferred to the light, the WDL3 protein is stabilized and involved in cortical MT reorganizations. (4) The

MT-severing protein complex katanin, which is composed of KTN80 and KTN1, severs MT to create new MT ends when irradiated with blue light.

(5) Plant conserved CLASP binds and stabilizes those new plus ends generated by katanin. Together, katanin and CLASP coordinate the rapid

transition of cortical MT transverse arrays to longitudinal arrays in response to blue light. (6) TON2 is required for light-induced MT array

reorganization by altering the ratio of branching to parallel MT-bound nucleation mediated g-tubulin complexes. In ton2 mutants, there are many

more parallel or de novo nucleation events than branched nucleation events.

investigation about the role of MTs in plant response to

salt stress.

Several MAPs have been functionally identified to

disturb the biphasic reorganization of cortical MTs

under salt stress, thereby promoting plant cell adaptation

to high salinity conditions. In response to salt stress,

SPR1 is cleared by the 26S proteasome, leading to the

fast depolymerization of cortical MTs [57,58]. Other

identified MAPs including CC (companion of cellulose

synthase) proteins, MAP65-1, WDL5 and RIC1,


probably participate in the cortical MT reorganization

under salt stress [59,60, 61�,62,63,64�]. The CC

proteins bind to the MTs and promote the bundling

through multiple MT binding motifs in its cytoplasmic

N-terminus, facilitating the MT reassembly and plant

survival under salt treatment [61�,65]. The MAP65-1

directly binds PA (phosphatidic acid) on the PM, which

consequently promotes its MT-stabilizing activity and

facilitates cortical MT recovery in high-salinity condi-

tions [66]. In contrast, WDL5 is directly targeted and

upregulated by a key transcription factor EIN3



(ETHYLENE-INSENSITIVE 3) in the ethylene sig-

naling pathway and is positively involved in ethylene-

mediated MT recovery under salt stress [64�,67]. It is

interesting that different regulatory mechanisms are

utilized by the MAPs, one controlling the activity of

MAPs through posttranslational regulation like ubiqui-

tination, while another accumulating MAPs through

transcriptional regulation by upstream signaling factors.

A third mechanism is the alteration of cellular localiza-

tion of MAPs under salt stress. Li et al. showed that salt

treatment activates ROP2, which resulted in the disso-

ciation of RIC1 from MTs and relocalization to the PM,

consequently favoring MT reassembly and seedling

survival [63]. These MAPs and related mechanisms have

been summarized into a simple model, showing how

diverse MAPs function differentially to regulate differ-

ent stages of MT disassembly, re-polymerization and

reorganization induced by salt stress (Figure 2).

Figure 2

Cell Wall

PlasmaMembrane

Cytoplasm

26

Ca2+

Salt Stress

+ end

Tubulin heterodimer

Phosphorylatedtubulin heterodimer

PHS1

CSI1CSC

WDL5

CC

RIC1SPR1

MAP65

GTP bound ROP2

GDP bound ROP2

Schematic model of biphasic MT reorganization in response to salt stress. T

MT disassembly (I) and MT repolymerization (II). Multiple MAPs are involved

and CC proteins localize on the PM under normal conditions. When treated

after that CC promotes cortical MT reassembly. (2, 4) Under salt stress, SP

to fast depolymerization of cortical MTs. (3) The a-tubulin is phosphorylated

polymerization-incompetent tubulin isoform and thereby promoting MT dep

relocalization of RIC1 to the PM and dissociation from MTs, consequently f

(PA) on the PM, thus promoting its MT-stabilizing activity and facilitating co

upregulated by a transcription factor EIN3 under salt treatment, and then W

depolymerization is associated with alteration of cytoplasmic Ca2+ levels, w


F-actin in salt response

The response of the actin cytoskeleton to salt stress is not

as well examined as that of MTs [24]. Short-term salt

stress induces actin cytoskeleton assembly and bundle

formation, but treatment over a longer time or with higher

salt induces actin cytoskeleton disassembly [68]. Such a

process of salt-induced actin dynamics could be regulated

by the SOS (salt overly sensitive) pathway and calcium

signaling, and in turn, function upstream to regulate

cytoplasmic calcium, as demonstrated by the study of

ARP2/3 (actin-related protein 2/3) [69�,70]. Zhao et al.showed that the mitochondria-dependent [Ca2+]cytincrease in response to salt stress is enhanced in mutant

arp2, resulting in its hypersensitivity to salt [69�]. How-

ever, how actin filaments are regulated by upstream

signals and the molecular mechanisms of certain ABPs

participating in salt stress adaptation remain largely

unknown and need to be further elucidated.

S proteosome

+ end+ end

Nucleus

WDL5


his figure illustrates the major MT reorganization process, including

to regulate the process. (1, 5, 7) Cellulose synthesis complex (CSC)

with salt, they are removed from the PM when MTs disassemble and

R1 is degraded by the 26S proteasome degradation pathway, leading

by PROPYZAMIDE-HYPERSENSITIVE 1 (PHS1), which generates a

olymerization under salt stress. (6) Activated ROP2 resulted in

avoring MT reassembly. (8) MAP65-1 directly binds phosphatidic acid

rtical MT recovery in high-salinity conditions. (9) Expression of WDL5 is

DL5 stabilizes and promotes MT recovery. (10) Salt-induced MT

hich in turn favors MT reassembly by unknown mechanisms.


90 Cell biology

Roles and mechanisms of the cytoskeleton instomatal movementF-actin in stomatal movement

Stomatal pores are formed by a pair of guard cells, which

have developed intrinsic mechanisms to swell or shrink,

promoting opening or closing of stomatal pores in

response to environmental cues [71]. Studies have dem-

onstrated that the cytoskeleton, especially actin fila-

ments, is extremely important in the process of stomatal

movement. An actin-stabilizing agent like jasplakinolide

can inhibit the stomatal closure induced by ABA (abscisic

acid) treatment, but latrunculin B can depolymerize actin

filaments and enhance stomatal closure [72,73]. Interest-

ingly, it was observed that radially oriented actin fila-

ments are dominant in open stomata, but longitudinal

arrays dominate closed stomata, indicating that the actin

cytoskeleton needs to undergo remodeling to control

stomatal movement [72,74].

Recent studies provided evidence that various ABPs par-

ticipate in actin remodeling during stomatal movement,

such as ADFs (actin depolymerizing factors) [6,75–78].

Zhao et al. demonstrated that the actin severing/depolymer-

ization activity of ADF4, and perhaps other subclass I

ADFs, could be inhibited by phosphorylation through

CKL2 (casein kinase 1-like protein 2) with ABA treatment

or under stresses, thus facilitating the reassembly of actin

filaments instomatal closure [79�]. Interestingly,expressionof ADF5, another ADF with actin-bundling activity, is

upregulated during ABA-induced stomatal closure

[77,80]. Its loss-of-function mutant adf5 shows delayed

stomatal closure and reduced survival rate under drought

stress. Similarly, a plant unique ABP SCAB1 (STOMATAL

CLOSURERELATED ACTIN BINDING PROTEIN1)

has also been identified to stabilize and bundle actin fila-

ments, mediating stomatal closure [78,81]. ARP2/3 is a

conserved complex for actin nucleation and branching. A

mutant of its subunit ARPC2, hsr3, has wider stomatal

aperture and is less sensitive to external stimuli like

ABA, which can be rescued by catastrophic drug-induced

depolymerization of actin filaments [76]. The authors pro-

posed that activated ARP2/3 might exert force to separate

actin bundles or decrease the actin monomer concentration

to facilitate depolymerization of actin filaments. Moreover,

another two studies offer additional mechanisms of ARP2/3

participating in ABA-induced stomatal closure, either

through the generation of hydrogen peroxide or mediating

the vacuolar fusion in guard cells [82,83]. Another interest-

ing study showed that the SCAR/WAVE complex which

activates the ARP2/3 complex is specifically required for

dark-induced stomatal closure in Arabidopsis, but not for

that induced by ABA and calcium chloride [84�]. Together,

these demonstrate the complicated roles of ARP2/3 during

stomatal movement. It is noteworthy that various ABPs in

different events, including actin depolymerization, bun-

dling, branching and nucleation, work together or specifi-

cally to keep the fine balance of actin remodeling and thus


stomatal movement in response to external stimuli. A

simple model has been proposed to show multiple ABPs

involved in signal-induced stomata closure (Figure 3).

MTs in stomatal movement

Cortical MTs have also been demonstrated to reorganize

and participate in the stomatal movement in response to

ABA and light [85,86]. Increased polymerization of corti-

cal MTs was observed as stomata opened, but cortical

MTs became destabilized as they closed. Accordingly,

depolymerizing of cortical MTs using the drug oryzalin

results in inhibition of stomatal opening, but stabilization

using the drug taxol delayed their closure [85]. Khanna

et al. showed that COP1-mediated tubulin degradation

participates in the ABA-induced MT destabilization and

stomatal closure [86]. So far the role of MT organization in

both guard cell opening and closure remains unclear and

the MAPs involved are still to be identified.

Roles and mechanisms of the cytoskeleton inplant response to biotic stressesAlthough lacking specialized immune cells, plants have

developed their own effective immune system against

microbial attacks and infections during evolution. Much

evidence has demonstrated that the plant cytoskeleton,

especially the actin filaments, play an indispensable role

in defense responses, and were well summarized in

several recent reviews [6,14,15�]. The MTs, as well as

actin–MT coordination for inter-organelle communica-

tions, also contribute to plant immunity [87–92]. In this

section, we focus on the actin cytoskeleton response and

some recent advances concerning the signal sensing of the

actin cytoskeleton during plant defense against biotic

stimuli.

Actin filaments have been observed to undergo rapid

remodeling when attacked by diverse pathogens.

When challenged with fungi and oomycetes, enhanced

actin bundling and polarization are formed toward pene-

tration sites. Innate immune signaling activated by bac-

terial and fungal microbe-associated molecular patterns

leads to increased density, longer filament length and

longer lifetime [6,93�,94,95]. During plant innate immu-

nity, ABPs including ADFs, CP (capping protein) and

profilin serve as the sensor of defense signaling and

regulate the actin cytoskeleton remodeling [6,96]. In

particular, the severing activity of ADF4 was inhibited

and adf4 mutants showed insensitive phenotype when

treated with bacterial elicitor elf26, but not with fungi

elicitor chitin, indicating its specificity toward different

elicitors [94]. In contrast, the mutant of another ADFfamily protein adf1 is insensitive to various elicitors with

no specificity [94]. How their activity is inhibited and how

such specificity is regulated are yet to be clarified.

Another inhibition target is the barbed-end binding pro-

tein CP which negatively regulates the actin dynamic. Its

mutant cp did not trigger the actin remodeling with



Figure 3

Cell Wall

PlasmaMembrane

Cytoplasmhsr3 mutant

opal5 mutant

opal5 mutant

WT

WT

Actin ARP2/3 complex

SCAR/WAVE complex

ADF4 ADF5

Phosphorylated ADF4

CKL2

SCAB1 Nucleus

DarkADF5


Schematic model of actin remodeling in plant guard cells in response to environmental stresses. This figure illustrates the major actin remodeling

process, including actin disassembly (I) and actin reassembly (II), to facilitate the stimulus-induced stomatal closure. Multiple ABPs are involved in

regulating actin remodeling. (1) Conserved ARP2/3 and SCAR/WAVE complexes cooperate to mediate the actin branching in wild-type cells. (2)

Possible explanations of the function of ARP2/3 in stomatal actin remodeling. Activated ARP2/3 might exert force to separate actin bundles or

decrease the actin monomer concentration to facilitate depolymerization of actin filaments. When ARP2/3 is genetically disrupted (hsr3 mutant),

the depolymerization of actin filaments is delayed. (3, 4) The mutants of SCAR/WAVE complex (opal5 mutant) showed delayed stomatal closure

specifically in response to darkness but not to other signals like ABA, indicating the alternative factors which might function to active ARP2/3. (5,

6) ADF4 could be phosphorylated by CKL2, and its actin-severing/depolymerization activity is inhibited, facilitating the actin reassembly process.

(7, 8) ADF5 and plant-specific SCAB1 further stabilize and bundle the actin filaments through dual actin-binding domains in a single protein (ADF5)

or dimerization (SCAB1), facilitating stomatal closure in response to drought stress.

treatments of multiple elicitors, showing higher suscepti-

bility to pathogens [95,97,98]. The barbed-end capping

activity of CP is inhibited by increased PA which releases

CP from actin filaments to the PM during PTI (pattern-

triggered immunity) [15�,95,99]. Additionally, the ROS

(reactive oxygen species) signaling could inactivate CP in

the defense process [98]. Similarly, a unique profilin

PRF3 in Arabidopsis was proved to negatively regulate

the actin polymerization and its mutant prf3 showed

higher sensitivity to pathogens [96]. Strikingly, prf3showed a significant increase in ROS generation when

treated with elf26 and flg22. These studies indicate that


the actin cytoskeleton functions both upstream and

downstream of pathogen-associated molecular pattern-

triggered ROS signaling, maintaining the fine regulation

of plant immune response.

The study of some beneficial bacteria is of special

interest to increase crop yield; for example, rhizobia

form a symbiotic interaction with host plants and

generate the nitrogen-fixing nodules in legumes

and some non-legume plants. The actin cytoskeleton

and specific ABPs have also been reported to perform

important functions during nodulation [100�,101–103].


92 Cell biology

Table 1

Representative cytoskeleton-associated proteins and their roles in plant environmental adaptation

PProteins Activities on cytoskeleton Biological functions in environmental signaling response References

a. MAPs (microtubule-associated proteins)

KTN1 ATP-dependent MT severing Creating new MT ends at crossovers, and driving the blue light-

induced MT reorientation

[34��]

CLASP Stabilizing MT plus end Stabilizing the newly generated plus ends by katanin, and driving

the blue light-induced MT reorientation

[36�]

TON2 Regulating MT nucleation Altering the ratio of branching to parallel MT-bound nucleation,

and required for light-induced reorganization of cortical MT arrays

[37]

MDP25 Destabilizing MTs Mediating the cortical MT reorganization from transverse to

oblique and longitudinal arrays in dark-to-light response

[38]

WDL3 Bundling MTs Modulating cortical MT reorganization in dark-to-light response,

and regulated by COP1-mediated degradation in the dark

[39,40��]

SPR1 Stabilizing MTs Degraded by the 26S proteasome, leading to the fast

depolymerization of cortical MTs in response to salt stress

[57,58]

MAP65-1 Bundling MTs Binding phosphatidic acid (PA) on the plasma membrane (PM),

and facilitating cortical MT recovery in high-salinity conditions

[66]

WDL5 Bundling MTs Upregulated by EIN3, and positively involved in ethylene-

mediated MT recovery under salt stress

[64�,67]

CC proteins Bundling MTs Facilitating the MT reassembly and plant survival under salt

treatment

[61�,65]

RIC1 Inhibiting MT transition from

shortening to

growing status

Re-localized to the PM by activated ROP2, thus favoring MT

reassembly and seedling survival under salt treatment

[63]

b. ABPs (actin-binding proteins)

CHUP1 Polymerizing cp-actin filaments Driving the chloroplast movements in response to blue light

irradiation

[46,47]

THRUMIN1 Bundling actin filaments Localized to the PM and regulated by light and phototropin, an

important link between light perception and dynamics of the actin

filaments

[48,49]

KAC proteins Regulating cp-actin filaments Mediating chloroplast anchoring to the PM and actin-based

chloroplast movement

[50,51]

ARP2/3 complex

Actin filament nucleation and

branching

1. Regulating mitochondria-dependent [Ca2+]cyt increase in

response to salt stress

[69�]

2. Participating in ABA-induced stomatal closure, either through

facilitating depolymerization of actin filaments, the generation of

hydrogen peroxide or mediating the vacuolar fusion in guard cells

[76,82,83]

ADF4

Severing/depolymerizing actin

filaments

1. Phosphorylated and inhibited by CKL2, thus facilitating the

reassembly of actin filaments during drought/ABA-induced

stomatal closure

[79�]

2. Participating in plant defense responses during both PTI and

ETI

[15�,94]

ADF5 Bundling actin filaments Upregulated during ABA-induced stomatal closure, and

promoting stomatal closure and plant survival under drought

stress

[77,80]

SCAB1 Bundling actin filaments Required for stomatal closure under drought stress [78,81]

SCAR/WAVE

complex

Activating ARP2/3 complex Required for dark-induced stomatal closure but not for that

induced by ABA and calcium chloride with a yet unknown

mechanism

[84�]

CP Binding the barbed end of actin

filaments to inhibit actin

polymerization and filament-

filament annealing

Required for actin remodeling in plant defense responses [95,97–99]

PRF3 Negatively regulating

actin polymerization

Required for plant defense responses to pathogens, and required

for ROS generation when treated with elf26 and flg22

[96]

The dynamic and combined architecture of filamentous

F-actin arrays, short F-actin fragments and actin dots,

were recently revealed by live-cell imaging in Medicagotruncatula, broadening our knowledge of the cellular

mechanisms of actin-mediated regulation in plant–

rhizobia interaction [100�].


Conclusions and perspectivesThe diversity and significance of the cytoskeleton in

plant adaptation to the environment are well recognized.

Current evidence supports that the regulation of the

cytoskeleton in response to signals depends on certain

cytoskeleton-associated proteins (MAPs and ABPs),



which could be regulated at transcription and protein

levels, or by the change in cellular locations (Table 1).

However, the connections between the core signaling

pathways and the cytoskeleton remain largely missing.

For example, under salt stress, whether and how the plant

cytoskeleton could be directly regulated by the SOS

signal transduction pathway is unclear [53��,104]. In ani-

mal cells, the Na+/H+ antiporter NHE1, a homolog of

SOS1, anchors actin filaments to the PM through direct

interaction with ERM (the ABPs ezrin, radixin and moe-

sin), which are lacking in plants [105]. Future work should

fill such gaps in diverse plant response processes.

Another major challenge is to unveil the detailed function

network of the plant cytoskeleton in environmental adap-

tation. The best-characterized function of MTs is to

direct cellulose deposition, and for actin is to mediate

intracellular transport [3,6]. Some recent evidence indi-

cated additional functions of the plant cytoskeleton such

as altering the cytosolic calcium level, altering ROS

signaling and changing organelle morphology

[53��,69�,96,106]. However, how these functions are

achieved remains largely unknown. What is more, how

these multiple function modes are incorporated together

by the cytoskeleton dynamics and reorganization in the

environmental adaptation also need to be explored in

further in-depth studies. In addition, it is necessary and

also interesting to investigate how the MT and actin

filaments coordinate to facilitate plant responses to envi-

ronmental signals.

Conflict of interest statementNothing declared.

AcknowledgementsThe authors thank Ming Yuan (China Agricultural University) and Jiejie Li(Beijing Normal University) for critical reading and comments on thearticle, the National Science Fund for Distinguished Young Scholars forDistinguished Young Scholars (31625005 to T.M.) and the National NaturalScience Foundation of China (31872821 to T.M. and 31872644 to X.W.) forfunding. We apologize to those colleagues whose works were not cited dueto space limitations.

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