ArticlePDF AvailableLiterature Review

The overlooked functions of trichomes: Water absorption and metal detoxication

December 2022
Plant Cell and Environment 46(3)

December 2022
46(3)

DOI:10.1111/pce.14530

Authors:

Cui Li

Northwestern Polytechnical University

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The ability of trichomes to absorb water and detoxify metals has important implications for plant growth, ecology, the environment, and agriculture. This review discusses the occurrence, mechanisms, and consequences of water absorption and metal detoxication by trichomes. Critical future research directions regarding these two functions of trichomes are also highlighted. Abstract Trichomes are epidermal outgrowths on plant shoots. Their roles in protecting plants against herbivores and in the biosynthesis of specialized metabolites have long been recognized. Recently, studies are increasingly showing that trichomes also play important roles in water absorption and metal detoxication, with these roles having important implications for ecology, the environment, and agriculture. However, these two functions Article of trichomes have been largely overlooked and much remains unknown. In this review, we show that the trichomes of 37 plant species belonging to 14 plant families are involved in water absorption, whilst the trichomes of 33 species from 13 families are capable of sequestering metals within their trichomes. The ability of trichomes to absorb water results from their decreased hydrophobicity compared to the remainder of the leaf surface as well as the presence of special structures for collecting and absorbing water. In contrast, the metal detoxication function of trichomes results not only from the good connection of their basal cells to the underlying vascular tissues, but also from the presence of metal chelating ligands and transporters within the trichomes themselves. Knowledge gaps and critical future research questions regarding these two trichome functions are highlighted. This review improves our understanding on trichomes.

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Received: 18 August 2022

Revised: 20 December 2022

Accepted: 28 December 2022

DOI: 10.1111/pce.14530

REVIEW

The overlooked functions of trichomes: Water absorption

and metal detoxication

Cui Li

|Yingying Mo

|Nina Wang

|Longyi Xing

|Yang Qu

Yanlong Chen

|Zuoqiang Yuan

|Arshad Ali

|Jiyan Qi

Victoria Fernández

|Yuheng Wang

|Peter M. Kopittke

School of Ecology and Environment,

Northwestern Polytechnical University,

Xi'an, China

Baoji Academy of Agriculture Sciences,

Baoji, China

College of Life Sciences, Hebei University,

Hebei, China

School of Forest Engineering, Technical

University of Madrid, Madrid, Spain

School of Agriculture and Food Sciences,

The University of Queensland, St Lucia,

Queensland, Australia

Correspondence

Cui Li and Yanlong Chen, School of Ecology

and Environment, Northwestern Polytechnical

University, Xi'an 710072, China.

Email: cui.li@nwpu.edu.cn and

ylchen8895@nwpu.edu.cn

Funding information

National Natural Science Foundation of China,

Grant/Award Numbers: NSFC, 32101838;

Fundamental Research Funds for the Central

Universities, Grant/Award Number:

D5000210898; Science Foundation for

Youths of Shaanxi Province,

Grant/Award Number: 2021JQ‐097

Abstract

Trichomes are epidermal outgrowths on plant shoots. Their roles in protecting plants

against herbivores and in the biosynthesis of specialized metabolites have long been

recognized. Recently, studies are increasingly showing that trichomes also play

important roles in water absorption and metal detoxication, with these roles having

important implications for ecology, the environment, and agriculture. However,

these two functions of trichomes have been largely overlooked and much remains

unknown. In this review, we show that the trichomes of 37 plant species belonging

to 14 plant families are involved in water absorption, while the trichomes of 33

species from 13 families are capable of sequestering metals within their trichomes.

The ability of trichomes to absorb water results from their decreased hydrophobicity

compared to the remainder of the leaf surface as well as the presence of special

structures for collecting and absorbing water. In contrast, the metal detoxication

function of trichomes results not only from the good connection of their basal cells

to the underlying vascular tissues, but also from the presence of metal‐chelating

ligands and transporters within the trichomes themselves. Knowledge gaps and

critical future research questions regarding these two trichome functions are

highlighted. This review improves our understanding on trichomes.

KEYWORDS

foliar water uptake, function, metal accumulation, metal detoxication, trichome,

water absorption

1|INTRODUCTION

Trichomes are epidermal structures that are found widely on plant

shoots (Hülskamp, 2004). Trichomes are extremely diverse in shape,

structure and size—they can be unicellular or multicellular, straight or

branched and capitate or stellate in shape. Depending upon whether

they have the ability to biosynthesize and secrete substances,

trichomes can be divided into non‐glandular and glandular trichomes

whereby glandular trichomes can biosynthesize, store and secrete

specialized metabolites (Werker, 2000). Often, non‐glandular tri-

chomes are unicellular and are common within the plant kingdom, in

contrast, glandular trichomes are typically multicellular, have a peltate

or capitate head, and are present in 20%–30% of vascular plant

species (Liu et al., 2020; Muravnik, 2021).

Trichomes have been investigated since the early 20th century,

with a rapid increase during the 1990s. Studies in the 20th century

were generally focused on the anatomy of trichomes (Carlquist,

1958; Ramaley, 1902), and the physiological interactions between

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trichomes and the surrounding environment (Johnson, 1975; Levin,

1973; Nielsen et al., 1984). Since the 21st century, most studies have

tended to focus on trichome morphogenesis (e.g., the non‐glandular

trichomes of Arabidopsis thaliana and glandular trichomes of Solanum

lycopersicum [Berhin et al., 2022; Guan et al., 2014; Pichersky et al.,

2006]) and on the metabolic network of glandular trichomes (e.g., the

regulation network for the production of artemisinin by the glandular

secretory trichomes of Artemisia annua [Maes et al., 2011; Xie et al.,

2021]). From these studies, many functions of trichomes have been

identified, with these functions generally falling into four broad

categories (Figure 1): (i) Protection of plants against abiotic stresses,

including against UV damage (Manetas, 2003), water repellence

(Fernández et al., 2011; Gutschick, 1999; Konrad et al., 2021) and

ozone resistance (S. Li et al., 2018; Oksanen, 2018); water absorption

(Eller et al., 2016; Raux et al., 2020) and metal detoxication (Blamey

et al., 2015; C. Li et al., 2021). (ii) Protection of plants against biotic

stress, including against herbivores and pathogens via physical

interference and the excretion of toxic or repellent chemical

compounds by glandular trichomes (Karabourniotis et al., 2020;

Peiffer et al., 2009; Pillemer & Tingey, 1976). (iii) Biosynthesis of

specialized metabolites, including the production of various func-

tional phytochemicals which could be used as fragrances, food

additives or pharmaceuticals (Celedon et al., 2020; Chen et al., 2017;

Schuurink & Tissier, 2020); and the production and emission of

volatile organic compounds for plant‐plant communications (Ninkovic

et al., 2021). (iv) Developmental roles, including the regulation of the

structure of the flower during flower development (Glover et al.,

2004; El Ottra et al., 2013; Tan et al., 2016); assisting with pollination

(Oelschlägel et al., 2009) and helping with the capture of prey in

carnivorous plants (Lin et al., 2021) (Figure 1).

For any given trichome, its functions depend upon not only the

plant species and the organ in which it is located, but also the

environment where they grow, the timing of activity and its structure

and chemical composition (Muravnik, 2021). Generally, trichomes of

plants from the same genus tend to have similarities in both

morphology and function (Glover et al., 2004). However, while

trichomes are governed by the genotype of the plant, the structure,

chemical constituents and functions of trichomes are greatly affected

by the environment given that they are ‘active sensors’and can

respond to various stimulations (Karabourniotis et al., 2020; Machado

FIGURE 1 The function of the trichomes. The trichome functions marked with ‘*’are the topic of the present review.

670

LI ET AL.

et al., 2022; Zhou et al., 2017). For example, Zhou et al. (2017) found

that mechanical stimulation of the non‐glandular trichomes of A.

thaliana can cause Ca

oscillations and apoplastic alkalisation in the

trichome base and the surrounding cells.

Of these various functions, some are well‐known and have been

well‐characterized. For example, the herbivory resistance function of

trichomes has been systematically studied, with this protection being

associated with the occurrence of the thick, hairy trichomes which

provide a physical barrier, the release of chemical repellents, the

production of calcium oxalate (present as raphides) and the presence

of phenolics within the trichomes which make it difficult for insects

to chew, and by inducing the expression of defense transcripts

when in contact with herbivores (Franceschi & Nakata, 2005;

Karabourniotis et al., 2020; Peiffer et al., 2009). By contrast, some

trichome functions have often been overlooked and are less studied.

In particular, the role of trichomes in the absorption of water and in

the detoxication of metals have received comparatively little

attention historically, although an increasing number of studies are

now demonstrating that trichomes are involved in foliar water uptake

(FWU) and plant metal detoxication (Eller et al., 2016; Raux

et al., 2020).

To shed light on these two lesser‐studied functions of trichomes

is of substantial interest, not only to better understand the

physiology, metabolism and biochemistry of the trichome itself, but

also because this information could potentially lead to new

possibilities in the use and management of plants. For example, the

absorption of water by the trichomes could potentially benefit plants

through multiple mechanisms, including by improving the leaf water

status (Eller et al., 2016; Fuenzalida et al., 2019), enhancing

photosynthesis (Simonin et al., 2009) and by increasing carbon

assimilation rates (Binks et al., 2019). In addition, given that the

frequency of drought events will likely increase in the future, such

leaf‐level effects could change plant hydraulics, improve plant growth

and adaptability and could ultimately influence the ecology

(Figure 2a). In a similar manner, understanding the detoxication of

metals by trichomes has important implications for both the

environment (e.g., phytoremediation) and agriculture (e.g., foliar

fertilisation) (Blamey et al., 2015; C. Li et al., 2021; F. Zhao et al.,

2000). Regarding the former (i.e., the importance of metal detoxica-

tion by trichomes in phytoremediation), metal compartmentalisation

and detoxification in the shoot has been shown to be a key process

for phytoremediation given that it determines the concentration of

the metals that can be accumulated without exerting a toxic effect,

with the trichomes being an important site for metal sequestration

and detoxification in some plant species (Rascio & Navari‐Izzo, 2011;

F.‐J. Zhao et al., 2022). For example, the concentration of Se in the

trichomes of the Se hyperaccumulator Astragalus bisulcatus has been

reported to be 7–11 times greater than that in the surrounding leaf

FIGURE 2 Implications of water

absorption and metal detoxication by

trichomes. (a) Water absorption by trichomes

affects plants and potentially influences

ecology. (b) The role of metal detoxication by

trichomes in plants in phytoremediation and

foliar fertilisation. [Color figure can be viewed

at wileyonlinelibrary.com]

THE OVERLOOKED FUNCTIONS OF TRICHOMES

671

tissue (Freeman et al., 2006), and the Ni in the trichomes of the Ni

hyperaccumulators Alyssum murale and Alyssum pterocarpum has

been reported to account for 15%–20% of the dry weight of their

entire leaves (Broadhurst, Chaney, Angle, Maugel, et al., 2004).

Further on, the trichomes of the As hyperaccumulator Pteris vittata

can accumulate 20% of As in weight (W. Li et al., 2005), and it was

found in a field trial experiment that growing P. vittata reduced the

soil As concentration from 41 to 25 mg kg

−1

within 3 years (Wan

et al., 2020). Similarly, metal accumulation in the trichomes is also

important in foliar fertilisation—it was found in sunflower (Helianthus

annuus) that the non‐glandular trichomes play an important role in

not only the absorption but also the subsequent translocation of the

foliar Zn fertilizer (C. Li et al., 2019,2021) (Figure 2b).

Critically, these two lesser‐studied functions of trichomes (i.e.,

the absorption of water and the detoxication of metals) are

potentially related to each other. For example, it has been shown

that foliar application of fertilizers (such as Zn) to improve plant

growth in agricultural production systems can result in the

accumulation of these elements within the trichomes (C. Li et al.,

2019,2021), and it is possible that the absorption of these soluble

nutrients and their subsequent accumulation in the trichomes occurs

because the trichomes are efficient at absorbing water. Therefore, in

this review, we focus on two of the lesser‐known functions of

trichomes: (i) water absorption and (ii) metal detoxification. In this

regard, many issues remain unclear, such as what kind of trichomes

can absorb water or play roles in metal accumulation and detoxifica-

tion? Are these functions associated with special structures of

trichomes or occur in some specific plant genera? What are the

mechanisms that underpin these two functions? We first summarize

the current knowledge of trichome water absorption and metal

detoxification, then discuss the underlying physiological and molecu-

lar mechanisms that provide these functions. Finally, the implications

of these functions are considered, and future outstanding questions

are proposed. By examining the role of trichomes in water absorption

and metal detoxification, this review contributes to a better under-

standing of trichomes, allows for clearer recognition on these two

overlooked functions and provides the possibility of better using

trichomes.

2|THEROLEOFTRICHOMESINWATER

ABSORPTION

2.1 |Trichome and FWU

The first report of water uptake through leaves is from 1767,

reported by Mariott. However, this received comparatively little

attention until 1857, when Duchartr questioned this finding and

initiated a debate among plant physiologists as to whether water

could actually be absorbed by leaves. By the 20th century,

experimental evidence had demonstrated that water can indeed be

absorbed and utilized by leaves (Duchartre, 1857; Schreel & Steppe,

2020; Stone, 1963; Yang et al., 2010). In recent years, there has been

a considerable increase in interest in FWU (Berry et al., 2019;

Dawson & Goldsmith, 2018; Fernández et al., 2021; Guzmán‐

Delgado et al., 2021; Holanda et al., 2019; Limm et al., 2009;

Schreel & Steppe, 2019; Wang et al., 2016). For example, it has been

reported that at least 233 plant species from more than 70 plant

families can absorb water directly through their leaf surface (Berry

et al., 2019; Schreel et al., 2022).

Given the importance of FWU to both the plants and the ecology

as mentioned above, the pathway of FWU has been examined in

relation to the leaf epidermal structures—the cuticle, stomata and

trichomes (Eller et al., 2013; Guzmán‐Delgado et al., 2021; Ray et al.,

2022). It was found that FWU can occur through both the cuticle and

the stomata, with the structure and chemical composition of the

cuticle affecting the water diffusion efficiency (Eller et al., 2013; Ray

et al., 2022). For the stomata, FWU likely occurs by the diffusion of

water vapour rather than as liquid flow (Guzmán‐Delgado et al.,

2021). In addition, it has been reported that water absorption can

also occur through the trichomes—it has been reported previously

that at least 11 plant species from six different families can absorb

water through their leaf trichomes (Guzmán‐Delgado et al., 2021),

with this suggesting that trichomes can potentially play a role in

FWU. Here, we consider existing studies that focused on the capacity

of trichomes to absorb water, with the mechanisms by which FWU

occurs through trichomes discussed.

2.2 |Studies examining water absorption by

trichomes

A total of 37 plant species belonging to 14 families and 12 orders

have been found to have trichomes that are involved in FWU

(Table 1). A variety of methods have been used to examine water

entering the leaf through trichomes, including the use of dye tracers

(Eller et al., 2016; Holanda et al., 2019; Losada et al., 2021; Pina et al.,

2016; Schreel et al., 2020; Vitarelli et al., 2016), radiolabeled water

tracers (Ohrui et al., 2007) and by comparing FWU in species

differing in trichome density (Z.‐L. Pan et al., 2021; Schwerbrock &

Leuschner, 2017). Of these 37 plant species, 15 belong to the

Bromeliaceae family and 6 belong to the Orchidaceae family. All

these 21 species are epiphytes, and hence their water and nutrient

uptake largely relies upon foliar absorption. Furthermore, the

trichomes involved in water absorption in the Bromeliaceae family

are similar in structure and morphology—they are all large peltate

wing‐shaped, multicellular non‐glandular trichomes (Figure 5). In

addition, for tank‐type atmospheric epiphytes, the peltate trichomes

on the leaf sheath (where water collects) have also been reported to

absorb water (Table 1). Apart from these 21 epiphytes, 9 of the

remaining 37 plant species (Opuntia microdasys,Tortula caninervis,

Capparis odoratissima, Croton erythroxyloides, Croton pygmaeus,

Croton splendidus, Combretum leprosum, Eremanthus erythropappus,

and Myrsine umbellata) from a range of other plant families that can

be categorized as either xerophytes or as plants that live in dry

habitats. In addition, trichome water absorption has also been

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LI ET AL.

TABLE 1 Trichomes involved in plant water absorption (the morphology of the trichomes listed in this table are shown in Figure 5)

Oder Family Species Trichome features Habitats References

Poales Bromeliaceae Tillandsia ionantha Peltate wing‐shaped trichome Epiphytes Ohrui et al. (2007)

Tillandsia usneoides Martin et al. (2013)

Tillandsia aeranthos

Tillandsia landbeckii

Raux et al. (2020)

Tillandsia streptophylla Peltate wing‐shaped trichome Epiphytes Benzing et al. (1976)

Tillandsia rigida Peltate wing‐shaped trichome Epiphytes Benzing et al. (1976)

Vriesea splenriet Peltate wing‐shaped trichome Tank‐type epiphytes Vanhoutte et al. (2017)

Vriesea galaxia

Neoregelia spectabilis Peltate wing‐shaped trichome on the leaf sheath Tank‐type epiphytes Benzing et al. (1976)

Billbergia pyramidalis Peltate wing‐shaped trichome on the leaf sheath Tank‐type epiphytes Benzing et al. (1976)

Aechmea bracteata Peltate wing‐shaped trichome on the leaf sheath Tank‐type epiphytes Benzing et al. (1976)

Guzmania monostachya Peltate wing‐shaped trichome on both the leaf

sheath and leaf blade

Tank‐type epiphytes Benzing et al. (1976)

Catopsis floribunda Peltate wing‐shaped trichome on both the leaf

sheath and leaf blade

Tank‐type epiphytes Benzing et al. (1976)

Vriesea glutinosa Peltate wing‐shaped trichome on both the leaf

sheath and leaf blade

Tank‐type epiphytes Benzing et al. (1976)

Brocchinia reducta Peltate wing‐shaped trichome on both the leaf

sheath and leaf blade

Tank‐type epiphytes Benzing et al. (1985)

Asparagales Orchidaceae Dendrobium bellatulum

Dendrobium cariniferum

Dendrobium draconis

Dendrobium longicornu

Dendrobium trigonopus

Dendrobium williamsonii

Hair‐like non‐glandular trichomes Epiphytic orchids Z.‐L. Pan et al. (2021)

Caryophyllales Cactaceae Opuntia microdasys Needle‐like and belt‐structured trichomes Xerophilous plant, fog collection Ju et al. (2012)

Pottiales Pottiaceae Tortula caninervis Hair‐like non‐glandular trichome Xerophilous plant, desert moss Z. Pan et al. (2016)

Brassicales Capparaceae Capparis odoratissima Peltate wing‐shaped trichomes Semiarid environments, fog collection Losada et al. (2021)

Euphorbiales Euphorbiaceae Croton erythroxyloides Peltate wing‐shaped trichomes Xeric environment, soil drought Vitarelli et al. (2016)

Croton pygmaeus Peltate wing‐shaped trichomes and stellate non‐

glandular trichomes

Croton splendidus Peltate wing‐shaped trichomes and fasciculate

trichomes

(Continues)

THE OVERLOOKED FUNCTIONS OF TRICHOMES

673

reported in a halophytic plant (Avicennia marina) that grows in salty

soils with low water availability. These trichomes have been found to

assist in capturing water from fog or dew to cope with water scarcity.

The structure and morphology of these trichomes vary greatly,

including belt‐structured, peltate, fasciculate, stellate, tector and hair‐

like trichomes (Table 1).

The observation that trichomes are involved in water absorption in

the above‐mentioned plants that are epiphytes or those which are

adapted to water‐limiting environments is perhaps not unexpected.

However, it has also been reported that plants grown in temperate

regions can absorb water via foliar trichomes (Fagus sylvatica)(Schreel

et al., 2020) and Mediterranean regions (Quercus ilex) (Fernández et al.,

2014), with this assisting the plants to gain water especially during

drought and when the leaves are wet (such as when dew is formed). In

addition, trichome water absorption has also been found in ferns

growing in highly humid environments (Polystichum braunii, Athyrium

filixfemina, Polystichum aculeatum,andDryopteris filix‐mas), but it must

be noted that this conclusion was derived by comparing the

relationship between trichome density in the pinnate fronds and foliar

water absorption rather than by direct evidence (Schwerbrock &

Leuschner, 2017). Finally, of the trichomes that have been identified as

being involved in water absorption, only those of M. umbellata and A.

marina are glandular trichomes (Table 1).

2.3 |Mechanisms of water absorption through

trichomes

The 15 Bromeliaceae species identified above all have large

multicellular peltate wing‐shaped non‐glandular trichomes (Ohrui

et al., 2007; Raux et al., 2020). For this type of trichome, it has been

found that the highly hygroscopic wing helps water accumulate at the

leaf surface by capillarity during wetting events, with the water then

flowing to the central foot cells before being driven inward by an

osmotic gradient (Raux et al., 2020). Furthermore, this water uptake

pathway is unidirectional—when the wetting event is finished and the

effective water potential of the environment falls below the water

potential of the foot cells, the thick cell wall of the trichome cells then

acts as a capillary wick and prevents outward flow and evaporation

(Raux et al., 2020). Interestingly, foliar water absorption through the

peltate trichomes of C. odoratissima (Losada et al., 2021) and C.

splendidus (Vitarelli et al., 2016) occurs in a manner similar to that

described for the peltate trichomes of the Bromeliaceae species. In

this regard, it has also been reported that the peltate wings of these

trichomes are rich in compounds with a high affinity for water, such

as pectic substances (pectin is a component of the primary cell wall

and comprises a wide variety of polysaccharides rich in galacturonic

acid, which can help maintain plant water status), while the basal cells

are rich in lipophilic substances (such as cutin) (Fernández et al.,

2021). Furthermore, trichomes are sometimes connected with

vascular tissues via idioblasts (Losada et al., 2021; Z. Pan et al.,

2016; Vitarelli et al., 2016), with this facilitating the translocation of

the absorbed water and improving further water absorption.

TABLE 1 (Continued)

Oder Family Species Trichome features Habitats References

Myrtales Combretaceae Combretum leprosum Peltate wing‐shaped trichomes Semiarid environments, dew collection Holanda et al. (2019); Pina

et al. (2016)

Asterales Asteraceae Eremanthus erythropappus Tector trichomes Soil drought, fog collection Eller et al. (2016)

Ericales Primulaceae Myrsine umbellata Peltate glandular trichomes Soil drought, fog collection Eller et al. (2016)

Fagales Fagaceae Fagus sylvatica Hair‐like non‐glandular trichomes Temperate regions Schreel et al. (2020)

Quercus ilex Mostly stellate non‐glandular trichomes Mediterranean regions Fernández et al. (2014)

Lamiales Acanthaceae Avicennia marina Pilate glandular trichomes Halophyte mangrove species Nguyen, Meir, P., Sack, et al.

(2017); Meir, P., Wolfe,

et al. (2017); Schaepdryver

et al. (2022)

Polypodiales Dryopteridaceae Polystichum braunii Morphology was not examined Woodland ferns, high air humidity Schwerbrock and Leuschner (2017)

Athyriaceae Athyrium filixfemina

Dryopteridaceae Polystichum aculeatum

Dryopteris filix‐mas

674

LI ET AL.

Together with the water absorption mechanism of trichomes of the

Bromeliaceae species (Raux et al., 2020), it can be concluded that

water absorption by these peltate trichomes occurs by the following

pathway: (i) the highly hydrophilic peltate wings are responsible for

holding water on the leaf surface during wetting events, (ii) the water

is driven inward by an osmotic gradient through the foot cells via the

apoplastic pathway, (iii) the lipid base of the trichomes prevents

water counterflow, and (iv) the sclereids or vascular cells connecting

the trichome base with the leaf vascular tissues provide translocation

of the absorbed water (Figure 3).

In a similar manner, the tector trichomes involved in water absorption

in E. erythropappus have also been found to have relatively high

hydrophilicity (Eller et al., 2016). In addition, a hair‐like trichome in F.

sylvatica (belonging to the Fagaceae family) growing in temperate regions

has also been reported to absorb water, likely due to the pectin‐rich

composition of the trichome and the non‐lignified cell wall which makes it

easier for water to penetrate (Schreel et al., 2020). This high water

sorption capacity of trichomes potentially results not only from their

special cuticle composition that makes them more hydrophilic, but also

because the phyllosphere microbes associated with the trichomes may

potentially produce biosurfactants and increase their water sorption

capacity (Remus‐Emsermann et al., 2011; Schlechter et al., 2019). Indeed,

the trichome surface is covered by a cuticle and its chemical composition

may differ significantly from the cuticle of the other leaf areas (Fernández

et al., 2021; C. Li et al., 2021).

Although peltate trichomes have been shown to play a role in water

absorption as discussed above, other kinds of trichomes can also be

important. For two desiccation‐tolerant xerophilous plants (O. microdasys

and T. caninervis), their trichome water absorption functions result from a

multiscale water harvesting system formed by the trichomes, with these

structures generating a strong capillary force that allows efficient water

collection and absorption from various wetting events, such as from

humid atmospheres, from fog or dew, and during precipitation (Ju et al.,

2012; Z. Pan et al., 2016). Another Fagaceae species, Q. ilex (holm oak), a

typical Mediterranean species, has stellate trichomes that also contribute

to FWU (Fernández et al., 2014). It has been suggested that these stellate

trichomes on the adaxial surface of the holm oak leaves increase the

adhesion of water to the leaf surface and that these trichomes are

connected with bundle sheath extensions in the leaf, with this facilitating

water absorption and translocation (Fernández et al., 2014).

Overall, it is apparent that the ability of trichomes to absorb water

depends upon: (i) a special water collection structure formed by the

trichomes to enable water collection during wetting events, (ii) a special

surface chemical composition (e.g., the cuticle of the trichomes possessing

high content of polysaccharides made it has a high affinity for water) that

enables wetting and adhesion of atmospheric water as a prerequisite for

water absorption, (iii) the osmotic pressure that allows water to enter the

leaf, especially to plants growing in xeric environments, (iv) the base of the

trichomes connecting with leaf vascular tissues favours the translocation

of the absorbed water, and (v) the lipid trichome base prevents outflow of

water (Figure 3).

Regardless, the relationship between trichomes and water is not

straightforward, and trichomes play contrasting roles in FWU (Berry

et al., 2019; Brewer et al., 1991). For example, it was found in some

studies that trichomes could promote water condensation on the leaf

surface and increase FWU (Konrad et al., 2015), whereas other

studies found that trichomes are water‐repellent which is often

recognized as one of the trichomes' protection functions (Brewer &

Smith, 1997; Konrad et al., 2021). This is because the interactions of

trichomes with water are influenced by a variety of factors, including

not only the special chemical and structural properties described

above, but also other factors such as trichome density, leaf

properties, water form (e.g., minute or macro droplets), the

pattern in which the water interacts with the trichomes (e.g., contact

angle), environmental conditions and physiological situations

(Roth‐Nebelsick et al., 2022).

3|THEROLEOFTRICHOMESINPLANT

METAL DETOXIFICATION

The detoxification of metals by plants is a critical process for growth

in environments containing elevated concentrations of metals, but

much remains unknown regarding the mechanisms by which plants

FIGURE 3 Water absorption by the

peltate wing‐shaped trichome based upon the

Bromeliaceae species (Raux et al., 2020),

Capparis odoratissima (Losada et al., 2021) and

Corton splendidus (Vitarelli et al., 2016). The

special structure and chemical composition

allow the trichomes to absorb water

efficiently. (a) Top view showing a peltate

wing‐shaped trichome which consists of a

wing and central foot cells. (b) Leaf cross

section showing the peltate trichome. [Color

figure can be viewed at

wileyonlinelibrary.com]

THE OVERLOOKED FUNCTIONS OF TRICHOMES

675

are able to accumulate and detoxify these metals within their tissues.

This accumulation and detoxification of metals are important in a

range of conditions, including for hyperaccumulators in ultramafic

soils, which contain high concentrations of metals such as Ni, acid

soils, which contain high concentrations of bioavailable metals such

as Al and Mn, and contaminated soils which contain high concentra-

tions of metals due to human activities. In such instances,

phytoremediation has been proposed as an approach for decreasing

the concentration of contaminants in soil due to their extraction,

accumulation and removal in the plant shoots (Beans, 2017;

Chaney & Baklanov, 2017; Oh et al., 2014). Here, we summarize

the plant species that have been reported to accumulate metals in

their trichomes, with the characteristics of the trichomes and the

mechanisms of metal accumulation and detoxification by the

trichomes also discussed.

3.1 |Studies examining metal accumulation in

trichomes

We have identified 37 studies examining metal accumulation in

trichomes (Table 2). These studies have been conducted for a wide

range of purposes, including for examining plant metal tolerance and

detoxication mechanisms (Choi et al., 2001;Čiamporová et al., 2021;

Iwasaki & Matsumura, 1999), observing metal distribution in plant

leaves (Ager et al., 2003; Lei et al., 2008) and for examining the

specific roles of trichomes in plant metal hyperaccumulation (W. Li

et al., 2005; Mcnear & Kupper, 2014; Ricachenevsky et al., 2021). In

addition, a variety of analytical approaches have been used to

investigate the accumulation of metals in the trichomes, including

scanning electron microscopy coupled with energy dispersive

spectroscopy (SEM‐EDS), synchrotron‐based X‐ray fluorescence

microspectroscopy (XFM), nuclear microprobe analysis and confocal

microscopy with specific fluorescence dyes (Ager et al., 2003;

Broadhurst, Chaney, Angle, Erbe, et al., 2004; Kozhevnikova

et al., 2014).

A total of 33 plant species from 13 families have been reported

to accumulate high concentrations of metals in their trichomes

(Table 2), with 61% of these 33 plant species belonging to the family

Brassicaceae. This is likely because, at least in part, the Brassicaceae

family is the second largest plant family of hyperaccumulators (the

first being Phyllanthaceae), especially for Ni hyperaccumulators

(Global Hyperaccumulator Database, 2022; Manara et al., 2020). As

a result, it is likely that more attention has been given to the

distribution of metal elements in this plant family, and correspond-

ingly, more species of this family have been observed to accumulate

metals in their trichomes. Apart from the Brassicaceae family, the

other plant families in which trichomes have been found to

accumulate metals are Acanthaceae, Asteraceae, Cannabaceae,

Cucurbitaceae, Fabaceae, Lythraceae, Moraceae, Polygonaceae,

Polypodiaceae, Pteridiaceae, Solanaceae and Violaceae, with two

plant species having been identified in Asteraceae whereas only one

plant species has been identified for the remaining families (Table 2).

For the trichomes of these 33 plant species, over 90% are non‐

glandular trichomes and more than 50% accumulate metals in the

base of the trichomes. In addition, it has been observed in some

species that the metals accumulate in the apoplast or cell wall of the

trichome basal cells. For example, in sunflower, Zn (C. Li et al., 2019)

and Mn (Blamey et al., 2018) are localized in the apoplast of the basal

cell of the non‐glandular trichomes, and in A. thaliana Cd is chelated

in the cell wall of the non‐glandular trichome basal cells (Gao et al.,

2021). A. marina,Rumex acetosella and Nicotiana tabacum are the only

three species where glandular trichomes have been found to

accumulate metals. Interestingly, the glandular trichomes of A. marina

and N. tabacum have also been found to excrete metals from

glandular trichomes, with enhanced Ca concentrations promoting this

excretion in N. tabacum (Choi et al., 2001;Čiamporová et al., 2021;

Macfarlane & Burchett, 2000). Across the 33 plant species, the

morphology and structure of the trichomes involved in metal

accumulation vary greatly, including trichomes that are ‘Y’shaped,

stellate, dendritic, simple branch shaped and ‘T’shaped (Table 2and

Figure 5). As discussed previously for water absorption, for plants

within the same genus, we find similarities in both trichome

morphology and their metal accumulation properties. For example,

within the Brassicaceae family, the Arabidopsis genus accumulates Cd

and Zn at the base of dendritic non‐glandular trichomes (Fukuda

et al., 2020; Guo et al., 2022; Isaure et al., 2015; F. Zhao et al., 2000),

while the Alyssum genus accumulates Ni and Mn in the base of the

stellate non‐glandular trichomes (Broadhurst, Chaney, Angle, Erbe,

et al., 2004; Ghasemi et al., 2009; Tappero et al., 2007).

The metals that accumulate in trichomes include Zn, Cu, Mn, Cd,

Ni, Co, Tl, Se, Sr, As and Pb, with Zn, Mn, Ni and Cd being the most

frequently identified metals. Regarding the sources of the metals,

most studies have examined the accumulation of metals in trichomes

following uptake by the roots, but for sunflower, the accumulation of

metals in the trichomes have been examined for both root uptake and

for foliar absorption (i.e., foliar fertilisation). Interestingly, the

accumulation of metals in trichomes has been reported not only in

hyperaccumulators and metal tolerant plants, but also in non‐

hyperaccumulator and non‐metal tolerant species, with 16 of the

33 species being hyperaccumulators and four being metal tolerant

species (Table 2).

3.2 |Mechanisms of metal accumulation

and detoxication in trichomes

It is of considerable interest to understand the mechanisms whereby

metals accumulate in trichomes. Firstly, it has been found that the

basal cells of the trichomes in which metals accumulate are generally

connected with the surrounding mesophyll or epidermal cells by

plasmodesmata, and that the trichome basal cells are generally

further connected with vascular tissues such as bundle sheath

extensions—these enable the translocation of metals in or out of the

trichomes (Čiamporová et al., 2021; C. Li et al., 2021). Secondly, once

the metals have been translocated into the trichome, they must then

676

LI ET AL.

TABLE 2 Trichomes involving in plant metal accumulation and detoxication (the morphology of the trichomes listed in this table are shown in Figure 5)

Family Species

Heavy

metals

Metal distribution

in the trichomes Metal sources

Whether hyperaccumulator

or metal tolerant plants References

Acanthaceae Avicennia marina Zn, Cu Zn and Cu were excreted out

from the pilate glandular

trichomes

Macfarlane and Burchett (1999,2000)

Asteraceae Helianthus annuus Mn, Zn Uniseriate non‐glandular

trichome base

Root uptake or

foliar

absorption

Mn tolerant plant Blamey et al. (1986,2018)

C. Li et al. (2021)

Picris divaricata Cd, Zn In the ‘Y’shaped non‐

glandular trichome

Root uptake Zn and Cd hyperaccumulator Hu et al. (2012)

Bauchan et al. (2014)

Brassicaceae Alyssum murale/

Odontarrhena

muralis

Ni, Mn, Co Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Broadhurst, Chaney, Angle, Maugel, et al. (2004); Mcnear and

Kupper (2014); McNear DH et al. (2005); Tappero et al.

(2007); Do Nascimento et al. (2020)

Alyssum fallcinium Ni, Mn Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Broadhurst, Chaney, Angle, Maugel, et al. (2004)

Alyssum pterocarpum Ni, Mn Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Broadhurst, Chaney, Angle, Maugel, et al. (2004)

Alyssum inflatum Ni Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Ghasemi et al. (2009)

Alyssum corsicum Ni, Mn Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Babaoğlu Aydaşet al. (2013); Broadhurst, Chaney, Angle,

Maugel, et al. (2004); Leigh Broadhurst et al. (2009)

Alyssum serpyllifolium Ni Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator De La Fuente et al. (2007)

Alyssum lesbiacum Ni Peripheral regions of the

stellate non‐glandular

trichomes

Root uptake Ni hyperaccumulator Baklanov (2011); Krämer et al. (1997); Smart et al. (2007)

Alyssum bertolonii Ni Base of the stellate non‐

glandular trichomes

Root uptake Ni hyperaccumulator Marmiroli et al. (2004)

Arabidopsis thaliana Cd, Zn Base of the dendritic non‐

glandular trichome

Root uptake Ager et al. (2003); Gao et al. (2021); Guo et al. (2022);

Ricachenevsky et al. (2021)

Arabidopsis halleri Cd, Zn Base of the dendritic non‐

glandular trichome

Root uptake Zn and Cd hyperaccumulator Fukuda et al. (2020); Sarret et al. (2009); F. Zhao et al. (2000)

Arabidopsis lyrata Cd, Zn Base of the dendritic non‐

glandular trichome

Root uptake Isaure et al. (2015); Sarret et al. (2009)

Biscutella laevigata Tl Middle of the uniseriate

non‐glandular trichomes

Root uptake Tl hyperaccumulator Wierzbicka et al. (2016)

(Continues)

THE OVERLOOKED FUNCTIONS OF TRICHOMES

677

TABLE 2 (Continued)

Family Species

Heavy

metals

Metal distribution

in the trichomes Metal sources

Whether hyperaccumulator

or metal tolerant plants References

Biscutella auriculata Cd Non‐glandular trichome base

(morphology was not

examined)

Root uptake Cd tolerant plant Peco et al. (2020)

Bornmuellera

emarginata

Mn Stalkless T‐shaped non‐

glandular trichome

Root uptake Hopewell et al. (2021)

Bornmuellera tymphaea Mn Stalkless T‐shaped non‐

glandular trichome

Root uptake Ni hyperaccumulator Hopewell et al. (2021)

Brassica juncea Cd Uniseriate non‐glandular

trichomes

Root uptake Salt et al. (1995)

Capsella bursa‐pastoris Ni, Zn Base of the stellate non‐

glandular trichomes

Root uptake Kozhevnikova et al. (2014)

Chinese cabbage Cd Base of the hair‐like non‐

glandular trichomes

Root uptake Guo et al. (2022)

Lepidium ruderale Zn Base of the unicellular non‐

glandular trichomes

Root uptake Kozhevnikova et al. (2014)

Odontarrhena

chalcidica

Ni Stellate non‐glandular

trichomes

Root uptake Ni‐hyperaccumulator Hopewell et al. (2021)

Cannabaceae Cannabis sativa Cu Hair‐like non‐glandular

trichome

Root uptake Arru et al. (2004)

Cucurbitaceae Cucurbita moschata Mn Uniseriate non‐glandular

trichome base

Root uptake Iwasaki and Matsumura (1999)

Fabaceae Astragalus bisulcatus Se Hair‐like non‐glandular

trichomes

Root uptake Se hyperaccumulator Freeman et al. (2006)

Lythraceae Trapa natans Mn Rod‐shaped pluricellular non‐

glandular trichome base

Root uptake Mn tolerant hydrophyte Baldisserotto et al. (2007)

Moraceae Morus alba Zn, Sr Uniseriate non‐glandular

trichome

Root uptake Katayama et al. (2013); Kesavacharyulu et al. (2004)

Polygonaceae Rumex acetosella Zn, Cu Capitate glandular trichomes Root uptake Čiamporová et al. (2021)

Polypodiaceae Microsorum pteropus Cd Unicellular non‐glandular

trichomes

Root uptake Cd tolerant plant Lan et al. (2019)

678

LI ET AL.

be detoxified. In this regard, organic ligands (to chelate with the metal

ions) and metal transporters (such as for the transport of the metals

into the vacuoles) play important roles. For example, using in situ

hybridisation, Foley and Singh (1994) demonstrated a pronounced

expression of metallothionein in the leaf trichomes of Vicia faba.

Later, transcriptome analysis in N. tabacum found that its trichomes

are the primary sites for the expression of genes encoding stress‐

related proteins such as antipathogenic T‐phylloplanin‐like proteins

and glutathione peroxidase. It was also observed that the concentra-

tion of glutathione (related to metal complexation and sequestration)

was higher in the trichome cells than in other types of leaf cells

(Harada et al., 2010). In a similar manner, in sunflower, it was found

that its non‐glandular trichomes have nine groups of metal‐chelating

ligands and nine groups of heavy metal transporters that are involved

in the Zn accumulation in the trichomes (C. Li et al., 2021). In addition,

the metal found in the apoplast or in the cell wall of the trichomes

could be in the secondary cell wall as it can provide chelating sites for

the metal ions (Gao et al., 2021). Together, these special physiological

structures and molecular properties enabled metals to accumulate

within trichomes (Figure 4). Regardless, these mechanisms have only

been explored in a few plant species. A broader understanding of

trichome's physiology, molecular characteristics and cellular metabo-

lism are necessary.

4|FUTURE RESEARCH PERSPECTIVES

We have identified plant species (and their trichomes) that are

involved in water absorption and metal accumulation and detoxifica-

tion (Tables 1and 2), but these lists will certainly increase over time.

TABLE 2 (Continued)

Family Species

Heavy

metals

Metal distribution

in the trichomes Metal sources

Whether hyperaccumulator

or metal tolerant plants References

Pteridiaceae Pteris vittata As Base and stalk of the pilate

trichome

Root uptake As hyperaccumulator W. Li et al. (2005)

Solanaceae Nicotiana tabacum Cd, Zn Cd or Zn can be excreted out

of the pilate glandular

trichomes

Root uptake Choi et al. (2001); Harada and Choi (2008);

Sarret et al. (2006)

Violaceae Viola principis H. de

Boiss.

Pb, As Prickle like non‐glandular

trichome

Root uptake Pb, As and Cd hyperaccumulator Lei et al. (2008)

FIGURE 4 Metal detoxification by the uniseriate non‐glandular

trichome of Helianthus annuus (C. Li et al., 2019,2021). The metal

detoxication function of this trichome results not only from the good

connection of their basal cells to their surrounding cells and the

underlying vascular tissues, but also from the presence of metal‐

chelating ligands and transporters within the trichomes themselves.

[Color figure can be viewed at wileyonlinelibrary.com]

THE OVERLOOKED FUNCTIONS OF TRICHOMES

679

Comparatively few studies have focused on these two functions of

trichomes and our current understanding of these two functions of

trichomes is still fragmented and further information still needs to be

acquired.

4.1 |Water absorption by trichomes

Of the 37 plant species found to absorb water through trichomes,

57% are epiphytes and 24% are plants that grow in water‐stressed

environments (Table 1). This suggests that the ability to absorb water

through trichomes is likely associated with exposure to abiotic stress.

Indeed, not all plant trichomes can absorb water. For example, the

egg‐beater‐like trichomes of the floating fern (Salvinia molesta) are

highly water‐repellent and can keep its leaves largely free from water

even when the leaf is immersed in water or during rainfall events

(Konrad et al., 2021; Roth‐Nebelsick et al., 2022). This again indicates

that the structure and function of trichomes can be highly variable

and likely evolved to assist plants to cope with a range of biotic and

abiotic stress factors. However, it is still unclear why plants growing

in high‐humidity environments also have trichomes that can absorb

water. In this regard, few studies have examined the water

absorption capacity of trichomes, and the mechanisms by which

trichomes absorb water have been investigated in only a limited

number of species. Hence, further studies are needed in plants

growing in different environmental scenarios and from different plant

taxa to get a better picture of their diversity.

Regarding the mechanisms by which water is absorbed by

trichomes, current research largely investigates at the organ‐and

chemical‐level (i.e., the physical structure of the trichomes as well as

the related structure to the leaves and the chemical composition of

the trichomes), whereas no studies have examined water absorption

at the protein‐and gene‐level. For example, aquaporins are channel

proteins that can facilitate the transport of water across the

membranes of plant cells (Maurel et al., 2015), yet it is unclear

whether the cell membrane of the water absorption trichomes has

any aquaporins. In addition, it has been reported that some genes

participate not only in trichome development, but also in stress

responses (Zhang, Liu, Wang, Yuan, 2021), yet it is unclear which

genes contribute to trichome water absorption. These research

aspects could be included in future studies to help elucidate the

mechanisms by which water is absorbed by trichomes, thus helping

improve our understanding of trichome water absorption and its

contribution to plant water economy.

It has previously been demonstrated that the water absorbed by

trichomes is translocated to other tissues within the plant where it is

then utilized (Ha et al., 2021; Waseem et al., 2021). Hence, it is clear

that the water that is acquired through the trichomes can be of

general benefit to plants. For individual plants, the absorption of

water through trichomes not only can improve the leaf water status

FIGURE 5 The morphology of the trichomes listed in Tables 1and 2

680

LI ET AL.

and drought resistance, but it also contributes broadly to plant

survival when growing in environments where water is scarce

(Figure 2a). Furthermore, at the ecosystem level, this absorption of

water through the trichomes is potentially of substantial importance

to both forest and agricultural ecosystems as drought events are

likely to continue to increase in severity in the future (Schreel &

Steppe, 2020) (Figure 2a). For instance, species with this special

water acquisition function could potentially be selected or bred for

use in low‐rainfall regions. In this regard, current studies mostly focus

on forest species, with the absorption of water by trichomes in crop

species requiring evaluation. For example, it may be possible to breed

crop cultivars that have a high density of trichomes that are capable

of absorbing atmospheric water to improve their drought resistance.

4.2 |Metal detoxication by trichomes

Of the 33 plant species for which metal detoxification has been

found to be important in trichomes, 61% are either hyperaccumu-

lators or metal tolerant species, suggesting that sequestration of

metals in the trichomes is an important plant metal detoxication

mechanism (Table 2). It has been estimated that perhaps one‐third of

all plant species are able to accumulate metals in their trichomes

(Broadhurst, Chaney, Angle, Erbe, et al., 2004; Hopewell et al., 2021;

Kozhevnikova et al., 2014). Furthermore, the accumulation of metals

in trichomes is also a mechanism used by leaves to adjust plant metal

homoeostasis. For example, it was found in sunflower that the foliar‐

absorbed Zn was stored in the non‐glandular trichome base when the

leaf Zn concentration was high, while it was translocated out of the

non‐glandular trichomes and moved to other parts of the leaf tissues

when the leaf Zn concentration was decreased (C. Li et al., 2021). In a

similar manner, it was observed in A. thaliana that increasing the leaf

metal concentration further increased the metal concentration in the

trichomes (Ricachenevsky et al., 2021). However, due to the limited

number of studies, our knowledge of the interactions between

trichomes and metals is still in its infancy. Further studies are required

to identify additional plant species having different types of

trichomes and to provide a comprehensive understanding of the

mechanisms involved in metal detoxification by trichome.

In addition, it has been found that trichome density can increase

greatly when plants are under metal stress. For example, Azmat et al.

(2009) found that the trichome density of Phaseolus mungo and Lens

culinaris increased after exposure to high concentrations of Pb, Choi

et al. (2001) found that the trichome density of tobacco increased

upon Cd stress and Čiamporová et al. (2021) found that the density

of glandular trichomes of R. acetosella increased under Zn and Cu

stress. In this regard, it is likely that trichomes are part of plant's

stress‐response system, with an increase in trichome density under

various stresses, including metal stress (C. Li et al., 2017). Yet

whether increasing in trichome density is a strategy that used by

plants to cope with metal stress is still unclear. It is known that the

various stress‐coping functions of trichomes are interlinked. For

example, Guo et al. (2022) found that mechanical stimulation of

trichomes (an imitation of herbivores) of A. thaliana upregulated

genes involved in Cd

ion detoxification and increased the Cd

concentration in the trichomes. In this regard, some authors have

proposed that the metals that accumulate in the trichomes are not

only for metal detoxification but also that plants could utilize these

metals as a herbivores defense mechanism (Boyd, 2007; Gao et al.,

2021; Stolpe et al., 2017). Continued research is needed to decipher

the interplay between metal detoxication by trichomes and the other

trichome functions, such as protecting against herbivores.

It has been proposed that glandular trichomes could be used as

breeding targets for improving crop resistance to herbivores (Glas et al.,

2012). Taking this approach into account, for those species (especially

hyperaccumulators) whose trichomes can accumulate metals, breeding a

new genotype that has a higher density of this type of trichome would

potentially improve the efficiency of phytoremediation. Indeed, Zhang,

Lu, Wang, Yan, & Cui (2021) found that knockout of NtCycB2

(a negative regulator for glandular trichome initiation) in N. tabacum

resulted in a higher density and larger heads of glandular trichomes and

enhanced plant Cd‐stress tolerance due to the excretion of calcium

oxalate crystals by this glandular trichomes. Therefore, a better

understanding of the morphogenesis of trichomes and the underlying

mechanisms of metal detoxication is essential for the optimal utilization

of these plants in phytoremediation. In this regard, there is a substantial

need for deciphering the development of the metal‐accumulating

trichomes. In addition, metal‐chelating ligands and transporters are two

important factors that affect metal accumulation in trichomes. To find

the key genes which regulate the biosynthesis of metal‐chelating ligands

and the expression of the related metal transporters is pivotal for using

genetic engineering approaches to improve the efficiency of phytoex-

traction (Kumar et al., 2022). For example, it was found in A. thaliana

that overexpressing the cytosolic O‐acetylserine(thiol)lyase gene

(Atcys‐3A) (i.e., enhancing cysteine biosynthesis) significantly improved

Cd accumulation in the leaf trichomes (Ager et al., 2003;Domínguez‐

Solís et al., 2004). However, information regarding specific genes of

metal‐chelating ligands and metal transporters remains largely unknown.

Future studies could use the newly developed EPIDERMALMORPH

method to examine the development of trichomes (Brown & Jordan,

2022)andthesingle‐cell spatial transcriptome technique to decipher

the key genes involved in trichome metal accumulation and detoxication

(Xia et al., 2022).

Finally, the non‐glandular trichomes of sunflower have been

found to accumulate both foliar and root absorbed Zn and Mn

(Blamey et al., 2015,2018; C. Li et al., 2021). This suggests that

trichomes can accumulate metals either taken up by the roots or by

the foliage either from the atmospheric or foliar application.

However, the majority of the existing studies have solely investigated

the distribution of metals in trichomes following uptake by roots

(either in soil or hydroponic system). Future investigations should

therefore include other plant species and further explore whether

their trichomes can accumulate metals absorbed by the foliage. If so,

plants having this ability could also be used, for example, for the

absorption of atmospheric metal pollutants in an environmental

context or for improving the efficacy of foliar fertilizers in agriculture.

THE OVERLOOKED FUNCTIONS OF TRICHOMES

681

4.3 |Interconnection of water absorption

and metal detoxification by trichomes

Although much remains unclear regarding these two functions, we

note that >90% of the trichomes having these two functions are non‐

glandular (Tables 1and 2). In addition, unsurprisingly, both of these

functions appear to largely result from the interaction of the plant with

its surrounding environment—over half of the plants that have water‐

absorbing trichomes are epiphytes, while over half of the plants with

trichomes involved in metal detoxication are hyperaccumulators or

metal tolerant plants (Tables 1and 2). Nevertheless, the range of plant

species found to have these two functions is highly variable. Indeed, A.

marina is the only plant species that has glandular trichomes involved

in both plant water absorption and metal detoxication (Tables 1and 2).

However, this could be due to the fact that most of the previous

studies focused on either water absorption via the trichomes or metal

detoxication by the trichomes, rather than examining both functions

simultaneously. In fact, these two functions could co‐exist, as they

both involve translocation processes—from the trichomes to the inner

leaf tissues for water absorption and vice versa for metal detoxication.

Further studies are required to determine the relationship between

these two important functions of trichomes.

BOX 1 Current knowledge

Water absorption by trichomes

•A total of 37 plant species from 14 families have been

found to have trichomes that can absorb water, with

57% of these 37 species being epiphytes and 24% being

either xerophytes or growing in a dry habitat.

•For trichomes involved in water absorption, although

95% are non‐glandular, their structure and morphology

vary greatly, with similarities observed for species within

the same family.

•The ability of trichomes to absorb water is determined

by their structure (e.g., a water collection structure while

having the base of the trichome connected to the leaf

vascular tissues), surface chemical composition (e.g., the

surface of water absorbing structures being more

hydrophilic), and osmotic pressure.

Metal detoxication by trichomes

•A total of 33 plant species from 13 families have been

reported to have trichomes that can accumulate metals

in their trichomes, with 61% of these 33 species

belonging to the family Brassicaceae and 48% being

hyperaccumulators. The most frequently identified

metals in the trichomes are Zn, Mn, Ni and Cd.

•For the trichomes of the 33 plant species that are

accumulating metals: >90% are non‐glandular trichomes,

and >50% have metals that accumulate in the base of

the trichomes.

•The ability of trichomes to accumulate and detoxify

metals is related to the special structure (i.e., the

trichome basal cells are well connected with the leaf

vascular tissues) and to the presence of metal‐binding

ligands and transporters within the trichomes.

BOX 2 Outstanding research questions

Water absorption by trichomes

•Water absorption by trichomes appears to be related to

the nutrient and water acquisition regime of the plant

(e.g., 57% of the species are epiphytes) or to abiotic

stress experienced by the plant (e.g., drought). However,

water absorption by trichomes has only been examined

in a limited number of plant species. To provide a better

understanding on the relationship between the ability of

trichomes to absorb water and the growth environment

of the plant, additional research is required to evaluate

further plant species from different taxa under a variety

of environmental conditions.

•A better understanding on the mechanisms controlling

the absorption of water by trichomes will enable better

use of trichomes having this function (e.g., to improve

plant drought resistance and benefit the broader

ecosystem during drought) and inspire novel biomimetic

materials or devices to collect atmospheric water. Yet,

most studies examining the mechanisms by which

trichomes absorb water have focused primarily on the

physical structure and the surface chemical constitution

of the trichomes. Systematic research is required to

explore the mechanisms by which trichomes absorb

water, especially giving consideration to the protein‐and

gene‐level.

Metal detoxication by trichomes

•Our current understanding regarding the role of

trichomes in plant metal accumulation and detoxication

remains in its infancy—it is necessary to examine a

broader range of trichomes in various plant species.

•Studies are required to determine whether trichomes

that accumulate metals via root uptake can also

accumulate metals following foliar absorption. If so, this

could be used to remove atmospheric metal pollutants

and improve the absorption of foliar fertilizers.

•Key genes related to the metal detoxicating ligands and

key metal transporters need to be identified, with

genetic engineering approaches potentially used to

improve the efficiency of phytoremediation.

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LI ET AL.

5|CONCLUSIONS

We show that the trichomes of 37 plant species from 14 families are

involved in water absorption, with 21 of these species belonging to

atmospheric epiphytes. These plants are found to various environments,

including water‐stressed and saline areas, but also in temperate,

Mediterranean and highly humid regions. Our current understanding of

the role of trichomes in water absorption is primarily based upon

observations of the physical structure and chemical composition of

trichomes. In regard to metal detoxification by trichomes, we show that a

total of 33 plant species from 13 families have been reported to

sequester metals in their trichomes, with 90% of these trichomes being

non‐glandular and over 50% accumulating metals in their trichome base.

The elements most frequently reported to accumulate in trichomes are

Zn, Mn, Ni and Cd. Of these 33 plant species, 16 are hyperaccumulators

and four are metal‐tolerant species. The ability to sequester and detoxify

metals in trichomes is attributed to not only the special structure of the

trichomes but also the elevated levels of metal ligands and transporters

within the trichomes (Box 1). Furthermore, trichomes seem also to play a

role in maintaining the leaf metal homoeostasis. However, our current

understanding on these two trichome functions remains limited. Studies

should focus on identifying more plant species and types of trichomes

that contribute to water absorption and metal detoxification, focusing on

examining the properties of trichomes at the chemical, genetic and

protein level to better understand the mechanisms associated with these

two trichome functions (Box 2).

ACKNOWLEDGEMENTS

This work was supported by National Natural Science Foundation of

China (NSFC, 32101838), and Science Foundation for Youths of

Shaanxi Province (2021JQ‐097). Support was also provided to Cui Li

through the Fundamental Research Funds for the Central Universities

(D5000210898).

CONFLICT OF INTEREST

The authors declare no conflict of interest.

DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were

created or analysed in this study.

ORCID

Cui Li https://orcid.org/0000-0001-9885-3674

Arshad Ali http://orcid.org/0000-0001-9966-2917

Jiyan Qi http://orcid.org/0000-0003-3541-5751

Peter M. Kopittke http://orcid.org/0000-0003-4948-1880

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The tgd5 Mutation Affects Plastid Structure and Causes Giant Lipid Droplet Formation in Trichomes of Arabidopsis

Article

Full-text available

Jan 2024

Trichomes, epidermal protrusions in terrestrial plants, play diverse roles in plant defense, metabolism, and development. Arabidopsis thaliana, a model plant with single-celled and non-glandular trichomes, is a valuable system for studying cell differentiation in plants. However, organelle biology in Arabidopsis trichomes is relatively underexplored. Using light and transmission electron microscopy, we investigated the phenotypes of intracellular structures in Arabidopsis trichomes caused by tgd5 mutations, which are known to disrupt lipid transfer from the endoplasmic reticulum to plastids and have a large impact on chloroplast morphology in pavement and guard cells. Significant phenotypic changes in the plastid structure were observed in tgd5 trichome cells, including the absence of plastoglobuli, the emergence of clusters of electron-dense particles in the stroma, and the possibly cup-shaped morphology of plastids. Additionally, the tgd5 mutations triggered the formation of giant, up to 15 µm in diameter, neutral lipid-containing droplets in the trichome cells, as revealed using histochemical staining with lipophilic dyes. These lipid droplets were substantially larger and more frequent in trichome cells than in other types of cells in tgd5. These findings highlight the role of TGD5 in maintaining plastid structure and implicate the unique activity of lipid metabolism in Arabidopsis trichomes.

How the Adequate Choice of Plant Species Favors the Restoration Process in Areas Susceptible to Extreme Frost Events

Article

Full-text available

Oct 2023

Citation: Viveiros, E.; Francisco, B.S.; Dutra, F.B.; de Souza, L.A.; Inocente, M.C.; Bastos, A.C.V.; Costa, G.F.L.d.; Barbosa, M.C.; Martins, R.P.; Passaretti, R.A.; et al. How the Adequate Choice of Plant Species Simple Summary: Climate change is putting pressure on many researchers to adopt measures that solve the problems caused. And these problems go beyond the increase in global temperature, which, consequently, is causing an imbalance in the various natural ecosystems that remain. One of the main alternatives to combat the effects of climate change is the recovery of natural areas, be they forests, pastures, wetlands, or mountains. For that, in addition to factors such as soil preparation and post-planting management, the selection of species is fundamental to guarantee the success of the restoration. However, with the ongoing environmental imbalance, several extreme events are occurring unexpectedly, which puts pressure on the survival of some species. Frost is one of these events, which occurs when minimum temperatures are recorded in certain regions, causing various types of damage to species. Thus, the objective of this work was to evaluate how this extreme event-frost-can modify the community based on the intrinsic characteristics of some species in an area under restoration and to identify which species can resist these extreme events. Abstract: This work aimed to evaluate the impacts caused by extreme frost events in an ecological restoration area. We grouped the species in three ways: (1) type of trichome coverage; (2) shape of the seedling crown; and (3) functional groups according to the degree of damage caused by frost. The variables of the restored area and species characteristics were selected to be subjected to linear generalization analysis models (GLMs). A total of 104 individuals from seven species were sampled. The most affected species were Guazuma ulmifolia Lam. (98% of leaves affected), followed by Cecropia pachystachia Trécul and Hymenea courbaril L. (both 97%), Inga vera Willd. (84%), and Senegalia polyphylla (DC.) Britton & Rose with 75%. Tapirira guianensis Aubl. was considered an intermediate species, with 62% of the crown affected. Only Solanum granulosoleprosum Dunal was classified as slightly affected, with only 1.5% of leaves affected. With the GLM analysis, it was verified that the interaction between the variables of leaf thickness (X 2 = 37.1, df = 1, p < 0.001), trichome coverage (X 2 = 650.5, df = 2, p < 0.001), and leaf structure culture (X 2 = 54.0, df = 2, p < 0.001) resulted in a model with high Biology 2023, 12, 1369. https://doi.org/10.3390/biology12111369 https://www.mdpi.com/journal/biology Biology 2023, 12, 1369 2 of 14 predictive power (AIC = 927,244, BIC = 940,735, X 2 = 6947, R 2 = 0.74, p < 0.001). Frost-affected crown cover was best explained by the interaction between the three functional attributes (74%). We found that there is a tendency for thicker leaves completely covered in trichomes to be less affected by the impact of frost and that the coverage of the affected crown was greatly influenced by the coverage of trichomes. Seedlings with leaves completely covered in trichomes, thicker leaves, and a funneled or more open crown structure are those that are most likely to resist frost events. The success of ecological restoration in areas susceptible to extreme events such as frost can be predicted based on the functional attributes of the chosen species. This can contribute to a better selection of species to be used to restore degraded areas.

Morphological screening and expression of droughtrelated genes P5SC1 and DREB1A in water-stressed pearl millet (Pennisetum glaucum) at the pre-fruiting stage

Article

Full-text available

May 2024

This study characterized 33 pearl millet accessions for drought tolerance and expression patterns of drought-related genes (P5CS and DREB1A) at the pre-fruiting stage. The accessions were evaluated for variability and screened for drought tolerance. Five weeks after sowing, we screened the pearl millet accessions for morpho-agronomic variability and to determine their tolerance to water stress over 14 days. From these screenings, we identified the most and least tolerant accessions (NGB00886 and NGB00885, respectively) for gene expression studies. To determine the expression pattern of the DREB1A and P5CS genes, RNA was extracted from leaf samples and converted to cDNA for analysis via quantitative real-time polymerase chain reaction. The study found significant variation (p > 0.05) in morphological traits among the pearl millet accessions. The principal component analysis showed three components accounted for over 90% of the variance. Additionally, there were significant (p < 0.01, p > 0.05) correlations among the plant growth attributes of the accessions. At genetic index 15, the accessions were grouped into five distinct clusters corresponding to their genetic similarities. Gene expression studies showed differences in the Ct values of the reference gene (ACT1) against the target genes. The expression pattern showed that DREB1A was up-regulated in the most tolerant and down-regulated in the least tolerant, while P5CS was up-regulated in both accessions. The study concluded that there are morphological variations among the accessions in response to water stress at the pre-fruiting stage, and the up- and down-regulation of DREB1A and P5CS genes are involved in the mechanism of regulation of water stress modulations in pearl millet. Key words germplasm; drought tolerance; pearl millet; quantitative real-time polymerase chain reaction; reference genes

Adaptasi Morfologi Trikoma pada Tillandsia sp. dalam Penyerapan Air

Article

Apr 2024

Tillandsia sp. merupakan tanaman hijau sepanjang tahun yang berasal dari Amerika Latin. Tanaman ini tergolong tanaman epifit dengan ciri khusus tidak memiliki akar tanah yang kokoh seperti tanaman pada umumnya. Bentuk adaptasi yang dilakukan dengan adanya trikoma yang berfungsi sebagai penyerapan air dan nutrisi sehingga Tillandsia sp . dapat tumbuh dengan baik. Berbagai macam bentuk trikoma dapat menyesuaikan dengan kondisi lingkungan yang ada, sehingga morfologi setiap jenisnya berbeda sebagai bentuk adaptasi . Melalui berbagai sumber ditemukan adanya perbedaan pada kerapatan trikoma serta panjang sel sayap â€œ wing cells â€ yang dimiliki oleh beberapa jenis Tillandsia sp. Ciri khusus yang dimiliki tanaman ini yaitu pada trikoma dan sel sayap berfungsi sebagai sistem penyerapan air untuk menggantikan fungsi dan peran akar.

Spatial variations in leaf trichomes and their coordination with stomata in Quercus variabilis across Eastern Asia

Article

Apr 2024
J PLANT ECOL-UK

Leaf trichomes are derived from epidermal cells and serve an important function in regulating leaf heat balance and gas exchange. Variation in leaf functional traits is critical for predicting how plants will react to global climate change. In this study, we aimed to investigate how leaf trichome densities vary along large geographic gradients and how they interact with stomata in response to environmental change. We investigated the leaf trichome densities of 44 Quercus variabilis populations in Eastern Asia (24°–51.8° N, 99°–137° E) and their correlation with climatic factors and stomatal traits. In addition, 15 populations were grown in a common garden to study their adaptive variation and coordination with stomata. The mean value of trichome density in situ conditions was 459.78 trichome mm−2 with a range of 325.79–552.38 trichome mm−2. Trichome density increased with latitude and decreased with longitude. Both temperature and precipitation reduced the trichome density. Moreover, trichome density was positively correlated with stomatal density whether in situ or in the common garden, and both increased with drought. Our results suggested that leaf trichomes possess highly adaptive variation and are in close coordination with stomata in response to climate change. Our findings provide new insights toward elucidating the interactions between leaf traits and the adaptive strategies of plants under climate change.

How and why do species break a developmental trade-off? Elucidating the association of trichomes and stomata across species

Article

May 2024
AM J BOT

Premise Previous studies have suggested a trade‐off between trichome density ( D t ) and stomatal density ( D s ) due to shared cell precursors. We clarified how, when, and why this developmental trade‐off may be overcome across species. Methods We derived equations to determine the developmental basis for D t and D s in trichome and stomatal indices ( i t and i s ) and the sizes of epidermal pavement cells ( e ), trichome bases ( t ), and stomata ( s ) and quantified the importance of these determinants of D t and D s for 78 California species. We compiled 17 previous studies of D t – D s relationships to determine the commonness of D t – D s associations. We modeled the consequences of different D t – D s associations for plant carbon balance. Results Our analyses showed that higher D t was determined by higher i t and lower e , and higher D s by higher i s and lower e . Across California species, positive D t – D s coordination arose due to i t – i s coordination and impacts of the variation in e . A D t – D s trade‐off was found in only 30% of studies. Heuristic modeling showed that species sets would have the highest carbon balance with a positive or negative relationship or decoupling of D t and D s , depending on environmental conditions. Conclusions Shared precursor cells of trichomes and stomata do not limit higher numbers of both cell types or drive a general D t – D s trade‐off across species. This developmental flexibility across diverse species enables different D t – D s associations according to environmental pressures. Developmental trait analysis can clarify how contrasting trait associations would arise within and across species.

TRANSPARENT TESTA GLABRA2 defines trichome cell shape by modulating actin cytoskeleton in Arabidopsis thaliana

Article

Feb 2024

The Arabidopsis (Arabidopsis thaliana) TRANSPARENT TESTA GLABRA2 (TTG2) gene encodes a WRKY transcription factor that regulates a range of development events like trichome, seed coat, and atrichoblast formation. Loss-of-function of TTG2 was previously shown to reduce or eliminate trichome specification and branching. Here, we report the identification of an allele of TTG2, ttg2-6. In contrast to the ttg2 mutants described before, ttg2-6 displayed unique trichome phenotypes. Some ttg2-6 mutant trichomes were hyper-branched, whereas others were hypo-branched, distorted, or clustered. Further, we found that in addition to specifically activating R3 MYB transcription factor TRIPTYCHON (TRY) to modulate trichome specification, TTG2 also integrated cytoskeletal signaling to regulate trichome morphogenesis. The ttg2-6 trichomes displayed aberrant cortical microtubules (cMTs) and actin filaments (F-actin) configurations. Moreover, genetic and biochemical analyses showed that TTG2 could directly bind to the promoter and regulate the expression of BRICK1 (BRK1), which encodes a subunit of the actin nucleation promoting complex suppressor of cyclic AMP repressor (SCAR)/Wiskott-Aldrich syndrome protein family verprolin homologous protein (WAVE). Collectively, taking advantage of ttg2-6, we uncovered a function for TTG2 in facilitating cMTs and F-actin cytoskeleton-dependent trichome development, providing insight into cellular signaling events downstream of the core transcriptional regulation during trichome development in Arabidopsis.

ELONGATED HYPOTCOTYL5 and SPINE BASE SIZE1 together mediate light-regulated spine expansion in cucumber

Article

Jan 2024
PLANT PHYSIOL

Plant trichome development is influenced by diverse developmental and environmental signals, but the molecular mechanisms involved are not well understood in most plant species. Fruit spines (trichomes) are an important trait in cucumber (Cucumis sativus L.), as they affect both fruit smoothness and commercial quality. Spine Base Size1 (CsSBS1) has been identified as essential for regulating fruit spine size in cucumber. Here, we discovered that CsSBS1 controls a season-dependent phenotype of spine base size in wild-type plants. Decreased light intensity led to reduced expression of CsSBS1 and smaller spine base size in wild-type plants, but not in the mutants with CsSBS1 deletion. Additionally, knockout of CsSBS1 resulted in smaller fruit spine base size and eliminated the light-induced expansion of spines. Overexpression of CsSBS1 increased spine base size and rescued the decrease in spine base size under low light conditions. Further analysis revealed that ELONGATED HYPOTCOTYL5(HY5), a major transcription factor involved in light signaling pathways, directly binds to the promoter of CsSBS1 and activates its expression. Knockout of CsHY5 led to smaller fruit spine base size and abolished the light-induced expansion of spines. Taken together, our study findings have clarified a CsHY5-CsSBS1 regulatory module that mediates light-regulated spine expansion in cucumber. This finding offers a strategy for cucumber breeders to develop fruit with stable appearance quality under changing light conditions.

Physiological and transcriptional analyses reveal the resistance mechanisms of kiwifruit (Actinidia chinensis) mutant with enhanced heat tolerance

Article

Feb 2024
PLANT PHYSIOL BIOCH

Leaf Cover: An Ecological Perspective of the Peculiar Type and Arrangement of Trichomes in Kaunia R.M. King & H. Rob. (Eupatorieae, Asteraceae)

Article

May 2024
INT J PLANT SCI

Premise of the Research. While carrying out a taxonomic revision of Kaunia, uncommon types of trichomes and arrangement of trichomes on the leaves of K. gynoxymorpha and K. pachanoi were observed. Moreover, the trichome arrangement is not usual for either Kaunia or most of Eupatorieae. In this study, we aim to describe the leaf blade trichomes and indumentum in these two species and discuss, together with other anatomical characteristics, their ecological role, and potential adaptation to arid environments. Methodology. We used traditional light microscopy, scanning electron microscopy (SEM), and fluorescence microscopy to examine leaf blade anatomical characteristics. Besides, we carried out histochemical techniques on the leaves of both studied species to determine the presence of cutinized cell walls which may influence apoplastic water flow in trichomes. Pivotal Results. Our results show two-armed trichomes in Kaunia gynoxymorpha that are unusual in the tribe Eupatorieae. The arrangement of glandular and non-glandular leaf trichomes of the two studied species in tufts of 3 to 10 trichomes, sunken in surface crypts, is also uncommon. Conclusions. These tufts of trichomes and other anatomical and histochemical evidence suggest that non-glandular trichomes and their arrangement in tufts in Kaunia gynoxymorpha and K. pachanoi provide adaptive advantages by combining physical, mechanical, and biochemical functions, thus protecting plants against drought and high light intensity among other adverse conditions.

No cell is an island: characterising the leaf epidermis using epidermalmorph, a new R package

Article

Full-text available

Nov 2022
NEW PHYTOL

The leaf epidermis is the interface between a plant and its environment. The epidermis is highly variable in morphology, with links to both phylogeny and environment, and this diversity is relevant to several fields, including physiology, functional traits, palaeobotany, taxonomy and developmental biology. Describing and measuring leaf epidermal traits remains challenging. Current approaches are either extremely labour‐intensive and not feasible for large studies or limited to measurements of individual cells. Here, we present a method to characterise individual cell size, shape (including the effect of neighbouring cells) and arrangement from light microscope images. We provide the first automated characterisation of cell arrangement (from traced images) as well as multiple new shape characteristics. We have implemented this method in an R package, epidermalmorph, and provide an example workflow using this package, which includes functions to evaluate trait reliability and optimal sampling effort for any given group of plants. We demonstrate that our new metrics of cell shape are independent of gross cell shape, unlike existing metrics. epidermalmorph provides a broadly applicable method for quantifying epidermal traits that we hope can be used to disentangle the fundamental relationships between form and function in the leaf epidermis.

Foliar Water Uptake Capacity in Six Mangrove Species

Article

Full-text available

Jun 2022

Foliar water uptake (FWU) is a mechanism that enables plants to acquire water from the atmosphere through their leaves. As mangroves live in a saline sediment water environment, the mechanism of FWU might be of vital importance to acquire freshwater and grow. The goal of this study was to assess the FWU capacity of six different mangrove species belonging to four genera using a series of submersion experiments in which the leaf mass increase was measured and expressed per unit leaf area. The foliar water uptake capacity differed between species with the highest and lowest average water uptake in Avicennia marina (Forssk.) Vierh. (1.52 ± 0.48 mg H2O cm−2) and Bruguiera gymnorhiza (L.) Lam. (0.13 ± 0.06 mg H2O cm−2), respectively. Salt-excreting species showed a higher FWU capacity than non-excreting species. Moreover, A. marina, a salt-excreting species, showed a distinct leaf anatomical trait, i.e., trichomes, which were not observed in the other species and might be involved in the water absorption process. The storage of leaves in moist Ziplock bags prior to measurement caused leaf water uptake to already occur during transport to the field station, which proportionately increased the leaf water potential (A. marina: −0.31 ± 0.13 MPa and B. gymnorhiza: −2.70 ± 0.27 MPa). This increase should be considered when performing best practice leaf water potential measurements but did not affect the quantification of FWU capacity because of the water potential gradient between a leaf and the surrounding water during submersion. Our results highlight the differences that exist in FWU capacity between species residing in the same area and growing under the same environmental conditions. This comparative study therefore enhances our understanding of mangrove species’ functioning.

When rain collides with plants - Patterns and forces of drop impact and how leaves respond to them

Article

Full-text available

Feb 2022

Raindrop impact on leaves is a common event which is of relevance for numerous processes, including the dispersal of pathogens and propagules, leaf wax erosion, gas exchange, leaf water absorption, and interception and storage of rainwater by canopies. The process of drop impact is complex, and its outcome depends on many influential factors. The wettability of plants has been recognized as an important parameter which is itself complex and difficult to determine for leaf surfaces. Other important parameters include leaf inclination angle and the ability of leaves to respond elastically to drop impact. Different elastic motions are initiated by drop impact, including local deformation, flapping, torsion, and bending, as well as ‘swinging’ of the petiole. These elastic responses, which occur on different time scales, can affect drop impact directly or indirectly, by changing the leaf inclination. An important feature of drop impact is splashing, meaning the fragmentation of the drop with ejection of satellite droplets. This process is promoted by the kinetic energy of the drop and leaf traits. For instance, a dense trichome cover can suppress splashing. Basic drop impact patterns are presented and discussed for a number of different leaf types, as well as some exemplary mosses.

The impact of raindrops on Salvinia molesta leaves: effects of trichomes and elasticity

Article

Full-text available

Dec 2021
J R SOC INTERFACE

The floating leaves of the aquatic fern Salvinia molesta are covered by super-hydrophobic hairs (=trichomes) which are shaped like egg-beaters. These trichomes cause high water repellency and stable unwettability if the leaf is immersed. Whereas S. molesta hairs are technically interesting, there remains also the question concerning their biological relevance. S. molesta has its origin in Brazil within a region exposed to intense rainfall which easily penetrates the trichome cover. In this study, drop impact on leaves of S. molesta were analysed using a high-speed camera. The largest portion of the kinetic energy of a rain drop is absorbed by elastic responses of the trichomes and the leaf. Although rain water is mostly repelled, it turned out that the trichomes hamper swift shedding of rain water and some residual water can remain below the 'egg-beaters'. Drops rolling over the tri-chomes can, however, 'suck up' water trapped beneath the egg-beaters because the energetic state of a drop on top of the trichomes is-on account of the superhydrophobicity of the hairs-much more favourable. The tri-chomes may therefore be beneficial during intense rainfall, because they absorb some kinetic energy and keep the leaf base mostly free from water.

Peltate trichomes in the dormant shoot apex of Metrodorea nigra, a Rutaceae species with rhythmic growth

Article

Oct 2022

In Metrodorea nigra, a Rutaceae species with rhythmic growth, the shoot apex in the dormant stage is enclosed by modified stipules. The young organs are fully covered with peltate secretory trichomes, and these structures remain immersed in a hyaline exudate within a hood‐shaped structure. Our study focused on the morpho‐functional characterization of the peltate trichomes and cytological events associated with secretion. Shoot apices were collected during both dormant and active stages and processed for anatomical, cytochemical and ultrastructural studies. Trichomes initiate secretion early on, remain active throughout leaf development, but collapse as the leaves expand; at this time, secretory cavities start differentiation in the mesophyll and secretion increases as the leaf reach full expansion. The subcellular apparatus of the trichome head cells is consistent with hydrophilic and lipophilic secretions. Secretion involves two vesicle types: the smaller vesicles are PATAg‐positive (periodic acid/ thiocarbohydrazide/ silver proteinate) for carbohydrates and the larger ones are PATAg‐negative. In the first phase of secretory activity, the vesicles containing polysaccharides discharge their contents by exocytosis with the secretion accumulating beneath the cuticle which detaches from the cell wall. Later, a massive discharge of lipophilic substances (lipids and terpenes/phenols) results in their accumulation between the wall and cuticle. The release of the secretions occurs throughout cuticular microchannels. Continued protection of the leaves throughout the shoot development is ensured by replacement of the collapsed secretory trichomes by oil‐secreting cavities. These findings bring new perspectives for understanding secretion regulation in shoot apices of woody species with rhythmic growth.

Genetic engineering of plants for phytoremediation: advances and challenges

Article

May 2022

Heavy metal and metalloid contamination of the environment due to natural processes, industrialization, and anthropogenic activities pose a serious problem, threatening the health of millions of people exposed to drinking water and crop plants grown in contaminated areas. The traditional remediation method often includes the removal of pollutants physically and their disposal, an expensive, non-specific process that renders the soil unfit for cultivation and other usages. Phytoremediation is a successful approach for various heavy metal and metalloid decontamination. Multiple biotechnological tools, including genetic alteration of plants, can be employed to strengthen the phytoremediation capacity. Plant genetic engineering for phytoremediation can be an effective approach to exploit potential genes involved in metal uptake, translocation, reduction, complexation, vacuolar sequestration, and volatilization. However, one needs to understand the mechanism of increased accumulation of heavy metals in hyperaccumulators and translate the findings into high biomass crop plants for sustainable cleansing of the environment. This review will discuss various genetic engineering approaches for intensifying the phytoremediation capacity of plants for heavy metal and metalloids (Cd, Pb, Cr, As, Se and Hg), highlighting the recent advances and their limitations. We will also highlight the molecular understanding of various regulatory and signaling molecules and their utilization in improving the phytoremediation potential of plants. The review will also evaluate various limitations and challenges of the genetic engineering approaches.

The single-cell stereo-seq reveals region-specific cell subtypes and transcriptome profiling in Arabidopsis leaves

Article

May 2022
DEV CELL

Understanding the complex functions of plant leaves requires a thorough characterization of discrete cell features. Although single-cell gene expression profiling technologies have been developed, their application in characterizing cell subtypes has not been achieved yet. Here, we present scStereo-seq (single-cell spatial enhanced resolution omics sequencing) that enabled us to show the bona fide single-cell spatial transcriptome profiles of Arabidopsis leaves. Subtle but significant transcriptomic differences between upper and lower epidermal cells have been successfully distinguished. Furthermore, we discovered cell-type-specific gene expression gradients from the main vein to the leaf edge, which led to the finding of distinct spatial developmental trajectories of vascular cells and guard cells. Our study showcases the importance of physical locations of individual cells for exerting complex biological functions in plants and demonstrates that scStereo-seq is a powerful tool to integrate single-cell location and transcriptome information for plant biology study.

Foliar water uptake does not contribute to embolism repair in beech ( Fagus sylvatica L.)

Article

Feb 2022

Background and Aims Foliar water uptake has recently been suggested as a possible mechanism for the restoration of hydraulically dysfunctional xylem vessels. In this paper we used a combination of ecophysiological measurements, X-ray microcomputed tomography (microCT) and cryo-scanning electron microscopy (cryo-SEM) during a drought treatment to fully evaluate this hypothesis. Key Results Based on an assessment of these methods in beech (Fagus sylvatica L.) seedlings we were able to (i) confirm an increase in the amount of hydraulically redistributed water absorbed by leaves when the soil water potential decreased, and (ii) locate this redistributed water in hydraulically active vessels in the stem. However, (iii) no embolism repair was observed irrespective of the organ under investigation (i.e. stem, petiole or leaf) or the intensity of drought. Conclusion Our data provide evidence for a hydraulic pathway from the leaf surface to the stem xylem following a water potential gradient, but this pathway exists only in functional vessels and does not play a role in embolism repair for beech.

Diffusion of Volatile Organics and Water in the Epicuticular Waxes of Petunia Petal Epidermal Cells

Article

Feb 2022

Plant cuticles are a mixture of crystalline and amorphous waxes that restrict the exchange of molecules between the plant and the atmosphere. The multicomponent nature of cuticular waxes complicates the study of the relationship between the physical and transport properties. Here, a model cuticle based on the epicuticular waxes of Petunia hybrida flower petals was formulated to test the effect of wax composition on diffusion of water and volatile organic compounds (VOCs). The model cuticle was composed of a n‐tetracosane (C24H50), 1‐docosanol (C22H45OH), and 3‐methylbutyl dodecanoate (C17H34O2), reflecting the relative chain length, functional groups, molecular arrangements, and crystallinity of the natural waxes. Molecular dynamics simulations were performed to obtain diffusion coefficients for compounds moving through waxes of varying composition. Simulated VOC diffusivities of the model system were found to highly correlate with in vtiro measurements in isolated petunia cuticles. VOC diffusivity increased up to 30‐fold in completely amorphous waxes, indicating a significant effect of crystallinity on cuticular permeability. The crystallinity of the waxes was highly dependent on the elongation of the lattice length and decrease in gap width between crystalline unit cells. Diffusion of water and higher molecular weight VOCs were significantly affected by alterations in crystalline spacing and lengths, whereas the low molecular weight VOCs were less affected. Comparison of measured diffusion coefficients from atomistic simulations and emissions from petunia flowers indicates that the role of the plant cuticle in the VOC emission network is attributed to the differential control on mass transfer of individual VOCs by controlling the composition, amount, and dynamics of scent emission.

Mechanosensation triggers enhanced heavy metal ion uptake by non-glandular trichomes

Article

Dec 2021
J HAZARD MATER

The trichomes of Arabidopsis thaliana serve as accumulation sites for heavy metals such as Cd²⁺, and thereby both help plants cope with heavy metal stress and detoxify the soil. These trichomes are also believed to prime plant defenses against insect herbivores in response to mechanical stimulation. Because Cd²⁺ in such trichomes may be beneficial for plant defenses, we hypothesized that mechanical stimulation would enhance sequestration of Cd²⁺ in trichomes. We quantified the distribution and concentration of Cd²⁺ in leaves of A. thaliana, of the glabrous mutant gl1-1 of A. thaliana, and Brassica rapa L. subsp. pekinensis (Lour.) Hanelt (Chinese cabbage) and examined how these changed following mechanical stimulation of the trichomes or leaves. Light brushing or exposure to caterpillars of Spodoptera exigua led trichomes of both A. thaliana and Chinese cabbage to accumulate Cd²⁺ complexes more rapidly and to a higher concentration than trichomes in unstimulated controls. Comparison to responses in leaves of gl1-1 mutants suggested that this acceleration and enhancement of Cd²⁺ storage requires signaling through trichomes. In wild type A. thaliana, Cd²⁺ was found exclusively in trichomes, whereas in gl1-1 mutants, Cd²⁺ was found mainly in the lef mesophyll cells. Results suggest a mechanobiological pathway for improving heavy metal detoxification of soils through the action of hyperaccumulator plant leaves containing non-glandular trichomes.

The overlooked functions of trichomes: Water absorption and metal detoxication

Abstract

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