Pce 12831

Plant, Cell and Environment (2017) 40, 858–871 doi: 10.1111/pce.
12831
Review
The functional role of xylem parenchyma cells and aquaporins

during recovery from severe water stress
Francesca Secchi1, Chiara Pagliarani1 & Maciej A. Zwieniecki2
1
Department of Agricultural, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco 10095, Italy and 2Department of
Plant Sciences, UC Davis, Davis, CA 95616, USA
ABSTRACT hydraulic conductivity. In recent years, significant efforts have

been made to gain knowledge on this debated process, but a
Xylem parenchyma cells [vessel associated cells (VACs)] con-
comprehensive understanding of the biological processes in-
stitute a significant fraction of the xylem in woody plants. These
volved in xylem recovery from embolism in tree stems remains
cells are often closely connected with xylem vessels or tracheids
elusive.
via simple pores (remnants of plasmodesmata fields). The close
This review explores recent research advances in woody
contact and biological activity of VACs during times of severe
plant embolism repair theories, which take into account the bi-
water stress and recovery from stress suggest that they are in-
ological processes occurring at stem and cellular levels.
volved in the maintenance of xylem transport capacity and re-
sponsible for the restoration of vessel/tracheid functionality
following embolism events. As recovery from embolism
requires the transport of water across xylem parenchyma cell XYLEM MORPHOLOGY AND PARENCHYMA
membranes, an understanding of stem-specific aquaporin CELLS IN WOODY PLANTS
expression patterns, localization and activity is a crucial part Long-distance water transport in vascular plants occurs
of any biological model dealing with embolism recovery through a network of conduits built from nonliving cells
processes in woody plants. In this review, we provide a short (xylem) along the stem, branches, twigs, petioles and leaf veins
overview of xylem parenchyma cell biology with a special focus that connect roots to leaf mesophyll cells (Sperry et al., 2003,
on aquaporins. In particular we address their distributions and Tyree & Zimmermann, 2002). The xylem represents about
activity during the development of drought stress, during the 99% of the entire length of the water transport pathway from
formation of embolism and the subsequent recovery from roots to photosynthetic tissues, and the remaining 1% consists
stress that may result in refilling. Complemented by the current of a few millimetres of extra-vascular pathways that water fol-
biological model of parenchyma cell function during recovery lows when moving from the root surface to the stele and from
from stress, this overview highlights recent breakthroughs on leaf minor veins to evaporation sites (Cruiziat et al., 2002,
the unique ability of long-lived perennial plants to undergo Nardini et al., 2011b).
cycles of embolism-recovery related to drought/rewetting or Xylem conduits are long hollow tubes with finite dimensions,
freeze/thaw events. dead at maturity (Carlquist, 2015, Comstock & Sperry, 2000).
They are characterized by thick and lignified walls capable of
INTRODUCTION sustaining large negative pressures (Hacke et al., 2001a,
Trees regularly cope with environmental stressors, many of Pittermann et al., 2006). Gymnosperms possess xylem conduits
which have been exacerbated recently by climatic alterations (tracheids) that are uniform in shape and length and connected
across the planet. Over the years, the plant physiology commu- to each other through small openings in the secondary cell
nity has focused increasing attention on drought stress, which is walls (bordered pits). Most conifers have a pit membrane struc-
known to induce a complex network of physiological effects in- ture with a porous margo and central torus assembly (Zimmer-
cluding the xylem embolism formation/recovery cycle. The way mann, 1983, Choat et al., 2008, Pittermann et al., 2005). In
in which plants sense and recover from embolism is a matter of Angiosperms, the water transport conduits are more special-
particular research interest because of its relevance to their in- ized vessels consisting of drum-shaped cells (vessel elements).
trinsic ability to handle the transport of water under tension. The end walls between vessels are open (perforation plates)
However, while embolism formation is a purely physical phe- with elements stacked end on end to form long tubes extending
nomenon related to xylem chemistry and morphology, xylem over several centimetres or even metres. Water transfer from
refilling requires the generation of water flow against a pres- vessel to vessel occurs through bordered pit-fields, which con-
sure gradient. Thus, recovery from embolism can only be un- sist of multiple small openings separating adjacent vessels with
derstood through consideration of biological activities thin cellulose/pectin membranes (Holbrook & Zwieniecki,
capable of providing the energy and water needed to restore 2005, Tyree & Zimmermann, 2002).
Tracheid and vessel elements are the key structural compo-
Correspondence: M. Zwieniecki. E-mail: [email protected] nents of long-distance water transport, but the xylem as a
858 © 2016 John Wiley & Sons Ltd
Response of xylem parenchyma cells to embolism 859
whole is not made of solely dead conduits. The bulk of second- of axial and radial parenchyma cells in wood may confer higher
ary xylem (functional xylem) contains, besides fibres, an inter- stem hydraulic capacitance. These properties – (1) facilitation
connected network of living cells that links heartwood of transport between phloem and xylem, (2) energy and os-
(non-functional xylem compartmentalized within the stem) motic storage capacity, and (3) water storage capacity – were
and phloem (stem parenchyma cells). These parenchyma cells the basis of the recently proposed role of stem parenchyma
usually have thin walls and are rectangular or square in shape cells as a crucial component in the maintenance of xylem trans-
(Morris et al., 2016). They are formed by fusiform and ray ini- port capacity and embolism removal (refilling) even under
tials of the vascular cambium and are oriented both axially small negative tensions (Nardini et al., 2011a, Nardini et al.,
and radially. The living parenchyma cells can represent a large 2011b, Salleo et al., 2004, Secchi & Zwieniecki, 2011,
component of the tissue volume and the abundance of those Zwieniecki & Holbrook, 2009). Specifics of the biology behind
varies across environments, plants organs and species and the role of parenchyma cells in embolism-recovery are
(Holbrook & Zwieniecki, 2005, Spicer, 2014). Stems have detailed in this review.
fewer, smaller and tighter ray parenchyma cells than the roots Although there is no single confirmed theory explaining the
(Denne & Gasson, 2008, Morris et al., 2016, Pratt et al., 2007). dynamics of embolism repair in all vascular plants, it is worth-
Moreover, recent meta-analysis has found significant differ- while noting that compared with angiosperms, gymnosperms
ences between volumes of ray and axial parenchyma across cli- tend to have little parenchyma in their wood. If we assume that
matic zones with higher volumes observed in tropical trees and the ability to rapidly repair embolisms relies on the presence of
lower volumes in trees and shrubs growing in temperate and nearby parenchyma cells, this may explain the long length of
subtropical areas (Morris et al., 2016). Conifers were found to conifer embolism recovery time (days or months) and their
have far less radial and axial parenchyma in xylem than angio- need for a larger safety margin when compared with angio-
sperms. Lianas and stem succulents represent some of the most sperms experiencing comparable levels of embolism (Johnson
parenchyma-rich stems in the plant world (Spicer, 2014), a pat- et al., 2012; Johnson et al., 2012). It is also proposed that coni-
tern that reflects an increased demand for mechanical elasticity fers may utilize an entirely different approach to embolism re-
in climbing plants and the need for water storage in succulents covery that depends on the tree’s ability to restore functional
(Brandes & Barros, 2008, Carlquist, 2015, Chapotin et al., 2006, water potentials when exposed to fog or snow (Earles et al.,
DeSmidt, 1922). 2016, Mayr et al., 2014). In this review, we will focus on the bi-
It is assumed that living parenchyma cells play many impor- ology of parenchyma cells in angiosperm species and discuss
tant functional roles. However, specific functions are often de- their biological role in xylem recovery from severe water stress.
rived indirectly as the location of these cells makes them
difficult to study. Among these functions, the loading/
unloading of solutes into/from the transpiration stream
PARENCHYMA FUNCTION IN XYLEM EMBOLISM
(De Boer & Volkov, 2003) and the storage and transport of
REPAIR
carbohydrates as soluble sugars, starch and/or lipids are most
often considered (Bucci et al., 2003, De Boer & Volkov, Water transport in the xylem is a purely physical process driven
2003, Salleo et al., 2004, Secchi et al., 2011, Spicer, 2014, by a difference in water pressure. Water transport through a
Zwieniecki & Holbrook, 2009). In addition, they may play a network of dead cellular conduits occurrs under negative pres-
significant role in defense against pathogens by preventing sures (tension). Because the apoplastic water column in the xy-
their lateral and axial spread (Deflorio et al., 2008, Morris & lem is under tension, it is considered to be in a metastable state
Jansen, 2016) and accumulating anti-microbial compounds. (Stroock et al., 2014) and at risk of cavitation. Although the ten-
Some evidence of their involvement in mechanical support is sions experienced by trees are far less than the tensions re-
also reported (attributed mostly to ray parenchyma) (Arbellay quired to cause homogeneous cavitation, they may be large
et al., 2012, Reiterer et al., 2002). enough to trigger cavitation from seeding sites – like the micron
Recent studies point to the role of living stem parenchyma or submicron-sized air pockets present in the vessel crevices
cells pathways between mature xylem and phloem, as xylem (Tyree & Sperry, 1989). Expansion of these gas bubbles results
conduits are both physically and functionally associated with in the formation of embolisms that can quickly spread through
living phloem. Physical association is derived from a single an entire vessel. Further spread of embolism from vessel to ves-
cambium initial that produces both xylem and phloem deriva- sel may occur via the penetration of air bubbles through bor-
tives (Larson, 1994); thus, the radially oriented parenchyma dered pit membranes (Brodersen et al., 2013). Embolism
cells grouped together in rays extend from xylem to phloem. formation is a purely physical process (Brenner, 1995, Tyree
This functional association is demonstrated by several exam- & Zimmermann, 2002) related to the degree of tension in
ples of the interchange of water and solutes between xylem the xylem, the chemical properties of water, the thermal envi-
and phloem (Metzner et al., 2010, Nardini et al., 2011b, ronment and the physical properties of the xylem (Hacke
Schneider et al., 1994, Vanbel, 1990, Wang et al., 1997). et al., 2001b, Holbrook & Zwieniecki, 1999, Stiller & Sperry,
Additionally, parenchyma cells are shown to be involved in 2002, Tyree & Zimmermann, 2002). The presence of an em-
water storage (as confirmed by the high amount of ray and ax- bolism disrupts the plant’s water continuum by reducing
ial parenchyma in stem succulents) and xylem hydraulic capac- xylem transport capacity and causing short and long-term
itance (Barnard et al., 2013, Holbrook et al., 2002, Pfautsch effects on plant functions. Effects include stomatal closure,
et al., 2015, Salleo et al., 2004). Therefore, a greater amount reductions in the rate of photosynthesis, reductions of growth,
© 2016 John Wiley & Sons Ltd, Plant, Cell and Environment, 40, 858–871
860 F. Secchi et al.
loss of production and even plant death (Brodribb & Cochard, adjacent to the xylem vessels, are at the forefront of the refilling
2009, Sperry et al., 1998). process (Salleo et al., 2004). This assumption is supported by
As the prolonged presence of embolisms is a threat for plant the observations of inhibition or reduction of refilling in the
survival, species have evolved several strategies to prevent case of either physical damage to phloem transport or the met-
and/or alleviate the effects of hydraulic failure and restore xy- abolic inhibition of living cells in stems (Bucci et al., 2003,
lem transport functionality. These include anatomical xylem Salleo et al., 2004, Zwieniecki et al., 2004). It was concluded that
adaptation (specialized pit membrane structures, stem phloem might be involved in supplying the energy to sustain
sectoriality and wood density), the shedding of leaves or small xylem recovery (Bucci et al., 2003, Salleo et al., 2004), and since
branches (shrubs) to lower evaporative demand and growing there is a physical separation of phloem from xylem conduits,
new vessels to replace nonfunctional conduits (Zwieniecki & living parenchyma cells can function as bridges that allow sol-
Secchi, 2015). These processes are very slow and necessitate utes (and water) to flow from phloem to embolized conduits
prolonged relief from water stress/transpirational demand. (Nardini et al., 2011a). This pathway may involve multiple
We might consider these long-term strategies non-competitive. crossings of cellular membranes, thus being mediated by the
However, some species growing in competitive environments activity of water channels (aquaporins), sugar transporters
demonstrate the evolution of active physiological strategies and plasmodesmata.
that lead to the quick recovery of xylem hydraulic functionality. Xylem parenchyma cells in contact with xylem conduits are
These strategies include (1) the generation of positive root assumed to simultaneously generate the energy gradient
pressure when the soil is fully saturated (often found only in (deposition of solutes in the form of sugars, ions or a combina-
small herbaceous and smaller woody plants) (Cochard et al., tion of both) that allows water to flow into empty
1994, Ewers et al., 1997, Yang et al., 2012); (2) access to external vessels/tracheids, and supply water for refilling (Zwieniecki &
water sources (rain, fog or snow) in order to facilitate water up- Holbrook, 2009). Regarding the first task, the initial research
take and water flow into the xylem through leaves, buds and/or focus has been on finding the source of osmoticum through
bark, a strategy adopted principally by coniferous species analysis of carbohydrates in the parenchyma cells and the role
(Earles et al., 2016, Laur & Hacke, 2014, Mayr et al., 2014); of phloem in the delivery of sugars to sustain refilling. Both en-
and (3) cellular activities of living xylem parenchyma cells, zymatic analysis and visualization techniques have demon-
resulting in fast (minutes to hours) localized embolism removal strated that starch levels in living parenchyma cells adjacent
in woody plants (observed primarily in angiosperm species) to xylem vessels decrease on a timescale coincident with embo-
(Brodersen & McElrone, 2013, Brodersen et al., 2010, Nardini lism refilling (Bucci et al., 2003, Nardini et al., 2011a, Sakr et al.,
et al., 2011b, Salleo et al., 2004, Secchi & Zwieniecki, 2012), 2003, Salleo et al., 2009, Secchi & Zwieniecki, 2011). Further-
which may even occur during the presence of active transpira- more, a drop in starch content has been associated with an in-
tion (Holbrook & Zwieniecki, 1999, Trifilo’ et al., 2003). The crease in parenchyma cell sucrose content (Nardini et al.,
presence of great tension most likely precludes the occurrence 2011a, Regier et al., 2009, Salleo et al., 2009, Secchi &
of xylem refilling, but recovery has been reported under low- Zwieniecki, 2010). These results are strongly supported by a
tension levels. Reconciling the presence of tension with embo- transcriptome analysis that found, in response to embolism,
lism recovery has been proved difficult to understand, and only both the down-regulation of genes transcribing the monosac-
recently in vivo imaging has suggested the ability of plants to charide metabolic pathways and the strong up-regulation of
refill embolized vessels in situations with very low tensions those involved in the disaccharide metabolic pathways that in-
(below 0.5 MPa) (Brodersen et al., 2010, Clearwater & Gold- clude starch metabolism (Secchi and Zwieniecki, 2011). Similar
stein, 2005, Knipfer et al., 2015, Zwieniecki et al., 2013). A re- changes in transcript expression were found in the petioles of
cent work using X-ray micro CT analysis has shown that in grapevine during cycles of water stress and recovery (Perrone
grapevine refilling can occur without presence of root pressure, et al., 2012b). Increased rates of starch depolymerization lead
and it is osmotically driven against low negative water potential to an upsurge of simple, low-molecular weight sugar concentra-
(Knipfer et al., 2016). However, despite scientific efforts tion that may be exported across membranes into the conduit
(Nardini et al., 2011a, Salleo et al., 1996, Secchi & Zwieniecki, wall establishing the gradient required to drive water move-
2010, Zwieniecki & Holbrook, 2009), the biological mecha- ment into the embolized vessel (Brodersen & McElrone,
nisms responsible for embolism recovery under low negative 2013, Nardini et al., 2011b, Secchi & Zwieniecki, 2012).
pressure are not resolved beyond the general statement that However, it has yet to be shown how the products of starch
living cells are involved in the recovery process. hydrolysis move from starch storing living cells in the stem to
Although embolism formation is a physical process, its re- vessel-associated parenchyma and finally to the walls of the
moval requires that empty vessels fill with water against conduit network. It has been recently proposed that this pro-
existing energy gradients as the bulk of water in the xylem re- cess of sugar movement might be controlled by tissue-level
mains under tension. In this scenario, recovery from embolism changes in stem chemistry (Fig. 1):
cannot happen spontaneously and necessitates (1) some physi-
ological activities in the xylem to maintain or restore transport • An increase in cellular sucrose concentration can be gener-
function (promoting water flow into empty conduits) and (2) ated by either the long-distance transport of sugars (mostly
the involvement of living parenchyma cells able to perform sucrose) through the phloem or from the hydrolysis of starch
physiological activities during the recovery process. Existing stored in the stem; hypothesis confirmed by Bucci et al.,
models of xylem repair suggest that living parenchyma cells, (2003), Nardini et al., (2011a), Salleo et al., (2004),
Figure 1. Schematic illustration of membrane transporter activity during onset of water stress and recovery (Secchi & Zwieniecki 2016). For details
of overall scenario describing stem parenchyma cell activity, please refer to the text.
Salleo et al., (2009), Secchi & Zwieniecki, (2011), and a novel in vivo technique, has just confirmed that during em-
Zwieniecki & Holbrook, (2009). bolism formation (induced water stress) xylem pH decreases
• Starch hydrolysis results in an increased symplastic cellular (Secchi & Zwieniecki, 2016)
soluble sugar concentration providing not only osmotic pro- • A drop in pH and thus the acidification of the apoplast may
tection from stress but also shifting the membrane sucrose stimulate the apoplastic activity of acidic invertases, promot-
gradient. This shift may trigger proton-coupled sucrose efflux ing the reduction of sucrose concentrations and at the same
into apoplastic compartments through the plasma membrane time increasing the accumulation of monosaccharides
sugar/proton co-transporters, as energized by membrane H+- (glucose and fructose; (Secchi & Zwieniecki, 2016) providing
ATPase (Geiger, 2011, Wippel et al., 2010); this hypothesis additional osmoticum for refilling.
has to be proved directly in plants, although an active • Lower apoplastic pH may trigger not only the activation of
proton-sucrose efflux has been demonstrated in heterolo- proton pumps but also the activation of metal ion antiporters.
gous systems (Carpaneto et al., 2005, Carpaneto et al., 2010). Xylem sap collected from embolized vessels in poplar
• Proton pumps have been localized in xylem-associated cells contained up to five times more the osmotic potential of func-
(De Boer & Volkov, 2003), and the chemical inhibition of tional vessels. Inorganic ions accounted for half of the
H+-ATPase pumps in parenchyma cells prevent recovery, osmoticum, and the rest was derived from soluble sugars
while the stimulation of their activities induces recovery (Secchi & Zwieniecki, 2012). Evidence of metal ion contribu-
(Salleo et al., 2004, Secchi & Zwieniecki, 2016), confirming tions to osmoticum is also provided by a previous study of
proton-coupled membrane transport. transcriptome analysis showing an increase in the expression
• Sucrose-proton efflux may have two effects: an increase in level of metal ion transporters in response to embolism for-
apoplastic sucrose concentration and a drop in apoplastic mation (Secchi et al., 2011). Thus, sugars and ions together
pH values. This hypothesis is supported by a previous report may account for the driving force that draws water into
showing that xylem sap collected from embolized vessels in empty conduits under low water stress [i.e. during recovery
poplar had a significantly lower pH than functional conduits from stress; (Secchi & Zwieniecki, 2012)]. Previously,
(Secchi & Zwieniecki, 2012). Alteration in pH is one of the CryoSEM showed concentration of solutes in the xylem sap
first chemical changes measurable in xylem sap from plants of maize in functional vessels in the range of ~100 mM
exposed to drought (Bahrun et al., 2002, Sobeih et al., (McCully et al., 2000; CryoSEM does not detect sugar) that
2004). Although the alkalization of sap is often measured in is osmotic levels similar to those observed in trees and ade-
transpiring plants (Wilkinson & Davies, 1997) and leads to quately high ~0.2 MPa to drive water into conduit under
the general conclusion that pH in xylem sap increases with low tension even if no sugar was present. It is worth to men-
water stress, a recent study showed that alkalization is not a tion that majority of herbaceous species undergo an
universal phenomenon. It has been demonstrated that in alkalization of apoplastic pH during stress conditions (Sharp
woody plants, xylem sap alkalization is much less common & Davies, 2009); therefore, sugar accumulation in the
than in annual species, and of the 22 species studied and ex- apoplast would be limited and other mechanisms of recovery
posed to water stress, only four showed an increase in sap from embolism might be in play. Thus, trees and crops might
pH (Sharp & Davies, 2009). Indeed, a new study, which uses adopt different strategies in order to recovery from embolism
formation where trees depend on local recovery while herba- (2015)]. Beyond single aquaporin type functions, further efforts
ceous plants on root pressure. have also recently improved our understanding of specific
• Mechanisms involved in embolism repair require that water interactions among AQP isoforms, such as PIP1 and PIP2
enters empty conduits and fills the entire lumen. Indeed, vi- members, especially in woody species. In this context, the
sual evidence from cryo-SEM studies, MRI observations quantification of expression changes in response to the im-
and CT-scans show that water reappears in previously empty posed stress of a single and/or multiple groups of AQP isoforms
conduits, confirming that plants do have the ability to remove coupled with studies on their tissue-specific localization is cer-
embolisms in the xylem (Clearwater & Goldstein, 2005, tainly a relevant strategy for obtaining experimental evidence
Holbrook et al., 2001, Scheenen et al., 2007, Zwieniecki about the physiological roles of aquaporins. Indeed, according
et al., 2013). Recently, in vivo imaging of grapevine with to Heinen et al., (2009) there are three main ways by which
high resolution x-ray computed tomography has shown that AQPs regulate water movement across cell membranes:
water droplets form on vessel walls in the proximity of pa- expression level, trafficking and gating. While all three are im-
renchyma cells and that these droplets expand until the lu- portant, expression analysis in particular is being used to guide
men completely refills (Knipfer et al., 2015, Knipfer et al., our understanding of the specific localization and activity of
2016, Brodersen et al., 2010). This evidence supports the diverse AQP isoforms. Despite their importance in all plant
prediction that parenchyma cells draw water into embolized species (annual and perennial) and all tissues, the majority of
conduits. investigations into AQP gene functions have been carried out
on herbaceous angiosperm species with special focus on leaves
In the proposed scenario, xylem parenchyma cells are the and roots [for details see the recent review by Maurel et al.,
primary means for restoration of hydraulic continuity in the xy- (2015)], considering the rest of a plant bulk tissue (i.e. total
lem. Although not previously tested, the amount of paren- xylem and bark). Studies of aquaporins in woody angiosperms
chyma cells, their relative contact with vessels and their and the localization of AQPs in ferns and gymnosperms are
physiological activity may be crucial in providing the energy much less explored. A current and comprehensive list of PIP1
for refilling. Preliminary support for this hypothesis has been and PIP2 isoforms expressed in woody plant tissues is reported
provided by Choat et al. (2015); the authors suggested that in Table 1. Several isoforms are tissue-specific, and some are al-
the lack of refilling in a conifer species (Sequoia sempervirens) most exclusively expressed in the xylem. However, phyloge-
could be attributed to the lower amount of parenchyma cells. netic analysis conducted on aquaporin sequences described in
However, new evidence suggests presence of refilling activity Table 1 show no obvious clustering (Fig. 2). The lack of a phy-
in the same species exposed to fog (Earles et al., 2016). In this logenetic signal most likely precludes a simple computational
case, radial parenchyma cells can provide path for water trans- approach to detect the AQPs responsible for the maintenance
port from the bark surface to tracheids. In addition, observa- of xylem hydraulic capacity.
tions that water droplets form on vessel walls in contact with The first indications of AQP presence in the stem of woody
axial/radial parenchyma cells suggest that these cells may be perennials was derived from gene expression studies con-
highly active in water transport. If so, we can assume that water ducted on poplar species. Among trees, poplar is certainly the
channel proteins (aquaporins) are critical to the refilling pro- best candidate for a woody model system for molecular biology
cess, and a closer look at aquaporin physiology is required to experiments addressing the functional characterization of
understand the potential for refilling in trees. genes such as aquaporins. Indeed, the genome of the species
Populus trichocarpa has already been fully sequenced and re-
leased (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.
AQUAPORINS AND THEIR LOCALIZATION IN THE
htm). In addition, these plants are relatively easy to genetically
STEM OF WOODY SPECIES
transform. Despite the overall limited information on AQP ac-
In all developmental phases and responses to environmental tivity in the stem, the majority of the available data have been
cues, the maintenance of water flow across membranes is regu- obtained on poplar. Although limited in scope, analyses have
lated by the activity and abundance of aquaporins (Hachez shown highly variable expression in different stem sections, at
et al., 2006). Five families of AQPs are known in higher plants different developmental stages and in response to stress treat-
on the basis of sequence similarities and common association ments, thus suggesting that stem AQPs are an important part
with peculiar cell membrane localization (Maurel et al., 2015). of stem biology in woody plants.
Among these, the PIP family, which is in turn divided For instance, significant insights on the expression profiles of
into two subfamilies, PIP1 and PIP2, is the most prolific; AQP isoforms were provided in poplar by Secchi et al., (2009).
examples can be found in woody plants, such as grapevine Along with transcripts of PIP1 and PIP2 members found in
and poplar, where 28 and 56 MIP-encoding genes have been roots and leaves, they have also been found in bark and xylem
identified, respectively (Fouquet et al., 2008, Gupta & samples of poplar stems, although with highly diverse mixes of
Sankararamakrishnan, 2009, Shelden et al., 2009). In the last isoform characteristics for each tissue. Detailed investigations
few years, MIP aquaporins were found to act as multifunctional into expression patterns of the previously characterized PIP1
pores; highlighting that AQPs are able to perceive a wide array and PIP2 genes in P. trichocarpa plants responding to water
of signals crucial to cell metabolism, nutrition and signalling stress and embolization events supports the idea that specific
cascades [for details see recent reviews by Bienert & xylem parenchyma AQPs are induced by stress and suggests
Chaumont (2014), Kaldenhoff et al., (2014), Maurel et al., some functional role of these proteins in dealing with drought,
Table 1. List of known PIP aquaporins expressed in woody plants with focus on stem aquaporins
Gene ID NCBI Response to

(a)
GenBank / Expression embolism/
(b)
Gene name Species Phytozome patterns recovery References
PtPIP1.1 Populus trichocarpa POPTR_0008s06580 (b) L (+++), R (++), ** (Secchi et al., 2009, Secchi & Zwieniecki,
W (++), B (+++) 2010, Secchi & Zwieniecki, 2011)
PtPIP1.2 P. trichocarpa POPTR_0003s12870 (b) L (++), R (++), no changes (Secchi et al., 2009, Secchi & Zwieniecki,
W (++), B (++) 2010, Secchi & Zwieniecki, 2011)
PtPIP1.3 P. trichocarpa POPTR_0010s19930 (b) L (+++), R (++), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (++)B (+++) 2010, Secchi & Zwieniecki, 2011)
PtPIP1.4 P. trichocarpa POPTR_0006s09920 (b) L (+), R (+), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (+), B (+) 2010, Secchi & Zwieniecki, 2011)
PtPIP1.5 P. trichocarpa POPTR_0016s12070 (b) L (++), R (++), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (++)B (++) 2010, Secchi & Zwieniecki, 2011)
PtPIP2.1 P. trichocarpa POPTR_0009s13890 (b) L (+), R (+), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (+), B (+) 2010, Secchi & Zwieniecki, 2011)
PtPIP2.2 P. trichocarpa POPTR_0004s18240 (b) L (+++), R (+++), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (+++), B (+++) 2010, Secchi & Zwieniecki, 2011)
PtPIP2.3 P. trichocarpa POPTR_0016s09090 (b) L (+), R (+), ** (Secchi et al., 2009, Secchi & Zwieniecki,
PtPIP2.4 P. trichocarpa POPTR_0010s22950 (b) L (++), R (++), * (Secchi et al., 2009, Secchi & Zwieniecki,
PtPIP2.5 P. trichocarpa POPTR_0006s12980 (b) L (+++), R (+++), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (++), B (+) 2010, Secchi & Zwieniecki, 2011)
PtPIP2.6 P. trichocarpa POPTR_0008s03950 (b) L (+++), R (++), ** (Secchi et al., 2009, Secchi & Zwieniecki,
PtPIP2.7 P. trichocarpa POPTR_0009s01940 (b) L (++), R (+++), * (Secchi et al., 2009, Secchi & Zwieniecki,
W (+), B (++) 2010, Secchi & Zwieniecki, 2011)
PtPIP2.8 P. trichocarpa POPTR_0005s11110 (b) L (+++), R (+), ** (Secchi et al., 2009, Secchi & Zwieniecki,
W (+), B (++) 2010, Secchi & Zwieniecki, 2011)
OePIP2.1 Olea europea L DQ202709 (a) L (+), R (+++), T (+) ** (Secchi et al., 2007a, Secchi et al., 2007b)
OePIP1.1 O. europea L DQ202708 (a) L (+), R (++), T (++) ** (Secchi et al., 2007a, Secchi et al., 2007b)
PttPIP2.1 P. tremula · tremuloides AJ849324 (a) L (++), S (++), (Marjanovic et al., 2005)
MR (++), FR (++)
PttPIP2.2 P. tremula · tremuloides AJ849325 (a) L (+), S (+), (Marjanovic et al., 2005)
MR (++), FR (+++)
MR (++), FR (+)
PttPIP2.4 P. tremula · tremuloides AJ849327 (a) L (++), S (+), (Marjanovic et al., 2005)
MR (+), FR (++)
PttPIP2.5 P. tremula · tremuloides AJ849328 (a) L (+), S ( ), (Marjanovic et al., 2005)
MR (+), FR (++)
MR (++), FR (+++)
PttPIP1.2 P. tremula · tremuloides AJ849322 (a) L (+), S (++), (Marjanovic et al., 2005)
MR (++), FR (++)
JrPIP2.1 Juglans regia AY189974 (a) L (+++), B (++), ** (Sakr et al., 2003)
W (++), R (+)
JrPIP2.2 J. regia AAO39008 (a) L (+++), B (+), ** (Sakr et al., 2003)
W (+), R (+++)
PtPIP2.3 Populus × ’Okanese’ 567607 (b) P (++), C (+++), ** (Almeida-Rodriguez & Hacke, 2012)
R(CC) (+++),
R(IC) (+)
PtPIP2.5 Populus × ’Okanese’ 826419 (b) P (++), C (+++), ** (Almeida-Rodriguez & Hacke, 2012)
R(CC) (+++),
R(IC) (+)
PgPIP1;1 Picea glauca BT113218 (a) R, L, S, W * (Laur & Hacke, 2014)
PgPIP1;2 P. glauca BT115139 (a) R, L, S ** (Laur & Hacke, 2014)
PgPIP1;3 P. glauca BT105794 (a) S, L (Laur & Hacke, 2014)
PgPIP2;1 P. glauca BT107672 (a) R, L, S * (Laur & Hacke, 2014)
PgPIP2;2 P. glauca BT105999 (a) R, L, S, W ** (Laur & Hacke, 2014)
PgPIP2;3 P. glauca BT115639 (a) R, S (Laur & Hacke, 2014)
PgPIP2;5 P. glauca BT108646 (a) reproductive parts (Laur & Hacke, 2014)
(Continues)
Table 1. (Continued)

(a)
(b)

PgPIP2;8 P. glauca BT106086 (a) R, L, S (Laur & Hacke, 2014)
(partial sequence)
PgPIP2;9 P. glauca BT106471 (a) S (Laur & Hacke, 2014)
CaPIP2;1 Coffea arabica LM654169 (a) L, R ** (Miniussi et al., 2015)
CaPIP2;2 C. arabica LM654170 (a) L, R ** (Miniussi et al., 2015)
ThPIP1-2 Tamarix ramosissima Unigene23675 (a) L * (Yan et al., 2015)
ThPIP2-1 T. ramosissima Unigene38680 (a) L * (Yan et al., 2015)
QpPIP2:1 Quercus petraea, JQ768372 (a) R (+++) (Rasheed-Rasheed-Depardieu et al., 2012)
Quercus robur
QpPIP2:2 Q. petraea, Q. robur JQ846268 (a) R (++) (Rasheed-Depardieu et al., 2012)
QpPIP2:3 Q. petraea, Q. robur JQ846269 (a) R (+) (Rasheed-Depardieu et al., 2012)
QpPIP1:3 Q. petraea, Q. robur JQ846272 (a) R( ) (Rasheed-Depardieu et al., 2012)
MusaPIP1;2 Musa acuminata FF561783 (a) L (++) (Sreedharan et al., 2013)
MusaPIP2;6 M. acuminata FL667907 (a) R, L (Sreedharan et al., 2015)
EcPIP1 Eucalyptus grandis XM_010057362.1 (a) L (+) (Tsuchihira et al., 2010)
EcPIP2 Eucalyptus XM_010033696.1 (a) L (+) (Tsuchihira et al., 2010)
camaldulensis
CsPIP1;1 Citrus sinensis orange1.1 g018895 (b) R (+), L (+++), (de Paula Santos Martins et al., 2015)
FL (+++),
CL (+++), F (+++)
CsPIP1;2 C. sinensis orange1.1 g023021 (b) R (+), L (+), FL (++), (de Paula Santos Martins et al., 2015)
CL (++), F (++)
CsPIP1;3 C. sinensis orange1.1 g023107 (b) R (+), L (+++), (de Paula Santos Martins et al., 2015)
FL (+++), CL (++),
F (++)
CsPIP1;4 C. sinensis orange1.1 g023069 (b) R (+), L (++), (de Paula Santos Martins et al., 2015)
FL (+++), CL ( ),
F (++)
CsPIP2;1 C. sinensis orange1.1 g023108 (b) R (+), L (+), FL( ), (de Paula Santos Martins et al., 2015)
CL ( ), F (+)
CsPIP2;2 C. sinensis orange1.1 g022966 (b) R (+), L (++), (de Paula Santos Martins et al., 2015)
FL (++), CL (++),
F (++)
FL (+++), CL (++),
F (+++)
FL (+++), CL (+),
F (+)
PpPIP1 Prunus persica AB303644 (a) Bu Cold stress (Yooyongwech et al., 2009)
PpPIP2 P. persica AB329725 (a) Bu Cold stress (Yooyongwech et al., 2009)
(partial seq)
VvPIP1;1 Vitis hybrid Richter-110 AF141643 (a) R (+++), RT (+++), (Baiges et al., 2001, Galmes et al., 2007)
L (+), S (+)
VvPIP1;2 V. hybrid Richter-110 AF141898 (a) R (+), RT (+), L (+), (Baiges et al., 2001, Galmes et al., 2007)
S (++)
VvPIP1;3 V. hybrid Richter-110 AF141899 (a) R (++), RT (++), (Baiges et al., 2001, Galmes et al., 2007)
L (+), S (++)
VvPIP2;1 V. hybrid Richter-110 AF141642 (a) R (++), RT (+++), (Baiges et al., 2001, Galmes et al., 2007)
L (++), S (++)
(Continues)
Table 1. (Continued)

(a)
(b)
VvPIP2;2 V. hybrid Richter-110 AF141900 (a) R (++), RT (+++), (Baiges et al., 2001, Galmes et al., 2007)
L (++), S (+++)
VvPIP1a Vitis vinifera cv. AF188844 (a) F (++) (Picaud et al., 2003)
Chardonnay, Ugny
Blanc, Pinot Meunier
VvPIP1b V. vinifera cv. AF188843 (a) F (++) (Picaud et al., 2003)
Chardonnay, Ugny
Blanc, Pinot Meunier
VvPIP1;1 V. vinifera cv. Cabernet DQ834694 (a) F (+) (Fouquet et al., 2008)
Sauvignon
Sauvignon
VvPIP1;3 V. vinifera cv. Cabernet DQ834696 (a) F (+++) (Fouquet et al., 2008)
Sauvignon
VvPIP2;1 V. vinifera cv. Cabernet DQ834698 (a) F (+++) (Fouquet et al., 2008)
Sauvignon
Sauvignon
VvPIP2;3 V. vinifera cv. Cabernet DQ834700 (a) F (++) (Fouquet et al., 2008)
Sauvignon
VvPIP1;1 V, vinifera diverse cvs EF364432 (a) R ( , cv Nebbiolo; ** (Chitarra et al., 2014, Perrone et al., 2012a,
++ cv. Grenache Perrone et al., 2012b, Pou et al., 2013,
and Chardonnay), Shelden et al., 2009, Vandeleur et al., 2009)
L (+), S ( ), P (++)
VvPIP1;2 V. vinifera diverse cvs EF364433 (a) R (+), S (++), P( ) * (Vandeleur et al., 2009, Perrone et al., 2012b,
Chitarra et al., 2014, Shelden et al., 2009)
VvPIP1;4 V. vinifera diverse cvs EF364435 (a) R (++) (Vandeleur et al., 2009, Shelden et al., 2009)
VvPIP2;1 V. vinifera diverse cvs AY823263 (a) R (+), L (++), S (++), ** (Vandeleur et al., 2009, Perrone et al., 2012a,
P (++) Perrone et al., 2012b, Chitarra et al., 2014,
Pou et al., 2013, Shelden et al., 2009)
VvPIP2;2 V. vinifera diverse cvs EF364436 (a) R (++), L (++), S (++) ** (Vandeleur et al., 2009, Perrone et al., 2012a,
Perrone et al., 2012b, Pou et al., 2013,
Shelden et al., 2009)
VvPIP2;3 V. vinifera diverse cvs EF364437 (a) R (+), L ( , cv. ** (Vandeleur et al., 2009, Perrone et al., 2012a,
Nebbiolo; ++, cv. Pou et al., 2013, Shelden et al., 2009)
Chardonnay)
VvPIP2;4 V. vinifera diverse cvs EF364438 (a) R (+) (Vandeleur et al., 2009, Shelden et al., 2009)
VvPIP2;4 N V. vinifera diverse cvs DQ358107 (a) R (+++), L (+), ** (Perrone et al., 2012a, Perrone et al., 2012b,
S ( ), P (++) Chitarra et al., 2014)
L, leaf; R, root; MP, main root; FR, fine root; RT, root tip; W, wood/xylem; B, bark; S, stem (wood and bark); T, twig; P, phloem (mainly in companion
cells); C, cambial zone and derivatives; R, ray parenchyma; R(CC), ray contact cells; R(IC), ray, isolation cells; Bu, buds; FL, flower; F, Fruit; CL,
Callus
+++, strong expression; ++, expression; +, detectable expression; , no expression
*not significant changes in gene expression
**significant changes in gene expression
embolism formation and recovery (Secchi et al., 2011, Secchi & in the expression of genes tied to carbohydrate metabolism
Zwieniecki, 2010, Secchi & Zwieniecki, 2011). In particular, and sugar transport (Secchi et al., 2011).
an analysis of the temporal dynamics of expression of all Similarly, in a work performed on grapevine plants (Vitis vi-
PIP1 and PIP2 transcriptional profiles, found a general strong nifera cv Grenache) subjected to either drought stress or artifi-
over-expression of the PIP1 subfamily when water stress oc- cially induced embolization, changes in the expression of
curred. However, response to embolism formation has re- diverse PIP1 and PIP2 aquaporin genes were profiled in both
sulted in the selective activation of only PIP1;1 and PIP1;3 petioles (whole tissue level) and also in vessel associated cells
genes in stem parenchyma (Secchi & Zwieniecki, 2010). (VACs) isolated from the same tissue samples using a laser
Genome-wide analysis of P. trichocarpa responding to embo- micro-dissection technique (Chitarra et al., 2014). Here, the
lism formation not only confirm the specificity of AQP ex- comparison of AQPs expression trends in a target cell type
pression patterns but also show a correlation with changes coupled with the transcriptional profiles of the same genes at
Figure 2. Neighbour-joining circle tree of the woody plant PIP1-type and PIP2-type aquaporin proteins detailed in Table 1. Only for Vitis
aquaporins, the letters 110R, F or S at the end of the protein name identify the aquaporins characterized by Baiges et al. (2001), Fouquet et al. (2008)
and Shelden et al. (2009), respectively. The significance of each node was tested using 2000 bootstrap replicates. Accession numbers of each aquaporin
are reported in Table 1 together with expression details and references. The green rectangular indicate, respectively, the specific PIP expression (++ or
+++) in xylem, purple in the phloem and red in entire stem tissue (bark and wood). The filled red rectangulars denote the presence of PIP expression
exclusively in stem tissue (it was not detectable in the other tissues tested).
the whole tissue level provided the first consistent information immunolabeling results showed that the strongest detection
about the specificity of some of these transcripts. Indeed, while of the two proteins occurred in the living parenchyma cells in
some of the VvPIP1 and VvPIP2-analysed genes were on the direct contact with xylem vessels (VACs), clearly attesting that
whole induced by stress and subsequent recovery in entire pet- during winter months these AQPs are specifically located in the
ioles, two transcripts encoding VvPIP1;1 and VvPIP2;4 N, VACs of walnut stems.
were exclusively activated in VACs, suggesting that the activity Subsequent tissue-specific and cell-specific localizations of
of the two derived proteins was restricted to these cells three AQP genes (two PIP2 isoforms and one TIP) in the sec-
(Chitarra et al., 2014). ondary xylem of hybrid poplar stems directly observed through
Although transcriptomic methods are certainly essential to in situ hybridization experiments (Almeida-Rodriguez &
the unravelling of AQP transcript alterations occurring in tar- Hacke, 2012) showed an increase in the abundance of all three
get organs or tissues during either plant phenological phases in parenchyma cells when drought or high N fertilization was
or the application of stress, they can only provide indirect evi- applied. This study validated and visually confirmed a previous
dence on the functional role of these genes. They do not supply work based solely on gene expression data (Hacke et al., 2010).
information about transcript localization. To better address the Drought and N fertilization resulted in significant changes in
characterization of aquaporins, the application of tissue and the abundance of target AQP transcripts in living tissues of
cellular level localization studies is pivotal. The first cellular de- the stem as well as in the ray cells adjacent to vessels (pith pa-
tection of AQPs in the stem of trees was in walnut (Juglans renchyma), with various degrees of changes in expression pat-
regia) plants experiencing winter embolism formation. The ex- terns depending on the applied treatment. Surprisingly, this
pression signal of two members of the PIP2 subfamily research revealed a strong increase in the AQP signal of paren-
(JrPIP2.1 and JrPIP2.2) was analysed by an immunolocaliza- chyma cells (often isolated) but only upon drought, suggesting
tion technique on several divisions of xylem tissue including an increased potential for water exchange between apoplast
vessels, fibres and parenchyma cells (Sakr et al., 2003). The and symplast in response to imposed external conditions.
Finally, AQP tissue-localization studies in non-angiosperms have revealed a fine-tuning of AQP expression in vessels asso-
(gymnosperms and ferns) are almost exclusively focused on ciated cells (VACs) especially during transition periods be-
leaves and gametophytes. For instance, interesting data were tween drought stress and stress recovery. It is thus believed
reported by Laur & Hacke (2014) in a study dealing with the that the physiological function of AQPs is specifically needed
analysis of aquaporin expression in the needles of Picea glauca, not during the imposition of environmental stress (drought
where the expression of PIP1 and PIP2 aquaporins was mea- and frost), but during the recovery from stresses that often
sured and compared with immunolocalization and in situ requires the restoration of xylem hydraulic conductivity.
hybridization experiments. The authors indicated that upon The contribution of aquaporins to the restoration of xylem
water deficit, all tested PIP genes were significantly down- hydraulic conductivity throughout periods of water stress
regulated in needles while a high humidity treatment resulted and/or subsequent recovery have mainly been addressed in
in an increased expression level for all transcripts, but to differ- order to better understand the plant water relations of distal
ent extents depending on the period of exposure. These results organs (roots and leaves) (Perrone et al., 2012a, Perrone
were confirmed by the diverse patterns of tissue localization et al., 2012b, Pou et al., 2013, Tsuchihira et al., 2010), whereas
obtained for each AQP. Indeed, while PIP1s were mainly local- a comprehensive understanding of AQPs in controlling xylem
ized in the endodermis, PIP2s showed a diffused signal within refilling in the stem is just emerging. Revisiting the insights
the central cylinder of the needle in both phloem tissue and gained from walnut stems in which expression was correlated
in transfusion parenchyma cells. It was suggested that PIP1 iso- with embolism recovery processes (Sakr et al., 2003), both
forms mainly regulate water transport across the bundle over-expression and an increased abundance of two walnut
sheath, from the needle epidermis towards the vascular tissue, PIP2 proteins was exclusively induced in winter months in the
while PIP2s may facilitate water movement from the needle VACs. This increase was simultaneous with an increase in the
towards stems (Laur & Hacke, 2014). These findings are sucrose concentrations of xylem sap and a decrease of starch
consistent with previous aquaporin immunolocalization exper- content in parenchyma cells (Sakr et al., 2003). It was assumed
iments carried out in P. abies, where a strong signal was de- that over-expression and increases in AQP abundance facili-
tected in needles at the vascular tissue level (Oliviusson et al., tate water flow from VACs into embolized vessels following
2001) and by observations of a higher abundance of PIP1 and this newly generated osmotic gradient. These results support
PIP2 aquaporins at the endodermis and phloem cell level in earlier observations of increased xylem water content, which
the needles of P. abies recovering from winter embolism (Mayr in parallel decreases in stem parenchyma water content
et al., 2014). Information on AQP expression in ferns comes reflecting the flow of water from cells to embolized vessels
from work conducted on the xerophytic fern Cheilanthes (Ameglio et al., 2001). Recently, additional reports have
lanosa (Diamond et al., 2012) where analysis indicated that highlighted the involvement of PIP2 genes in particular in facil-
the role of PIP1 proteins is highlighted by the maintenance of itating the recovery process (Table 1). For instance, the in-
water balance during gametophyte stages. creased abundance of PIP2;3 and PIP2;5 detected in the
Despite limited information, we can conclude that AQPs are VACs of drought-exposed poplar stems (Almeida-Rodriguez
abundant in living cells associated with long distance transport & Hacke, 2012) and the over-expression of PIP2;4 N and
tissue, including xylem axial and radial parenchyma and PIP2;1 genes observed in the VACs of either embolized or re-
phloem. It is also apparent that the expression of stem AQPs covering grape petioles (Chitarra et al., 2014) may both support
is related to plant hydraulic status with drought causing the need for PIP2 activity during vessel refilling along the
species/tissue specific up or down regulation and recovery from xylem-VAC-phloem transport path. These observations are in
stress (rain, re-watering and fog) causing significant up- agreement with the current models of embolism repair involv-
regulation of stem specific AQPs. This pattern of expression ing the interaction of xylem and phloem cells (Nardini et al.,
underlines the potential role of AQPs in the recovery of the hy- 2011a, Secchi et al., 2011, Secchi & Zwieniecki, 2016) presented
draulic capacity of the xylem, a trait that long-lived perennial here (Fig. 1).
plants may rely upon for their survival. The contribution of PIP1s to water stress and recovery in
trees was initially less considered as, unlike PIP2s, PIP1s were
thought to have little to no water transport activity when indi-
PARENCHYMA AQUAPORINS AND RECOVERY
vidually expressed in Xenopus oocytes (Chrispeels et al.,
FROM WATER STRESS
2001). This implied that PIP1 proteins did not work as water
Existing models of recovery processes occurring in trees indi- channels, and it was consequently assumed that they were not
cate that, among other functions, living parenchyma cells asso- necessary for promoting transmembrane water flow. Neverthe-
ciated with xylem conduits are key players in both supplying less, it was later shown that membrane water permeability sig-
the water and generating the energy needed to refill non- nificantly increased when PIP1s were co-expressed with PIP2s,
functional vessels (Brodersen & McElrone, 2013, Nardini implying a physical interaction between the two (Fetter et al.,
et al., 2011b, Salleo et al., 2004a, Zwieniecki & Holbrook, 2004, Secchi et al., 2009, Zelazny et al., 2007). Interestingly, only
2009). As water flow between the symplast and apoplast is me- PIP1 genes were shown to undergo strong transcriptional in-
diated by aquaporins, xylem parenchyma cells possess a signif- crease upon water stress and embolism formation in poplar
icant ability to temporally and spatially control water efflux, by stems (Secchi et al., 2011, Secchi & Zwieniecki, 2010, Secchi
regulating the expression and activity of specific AQP isoforms. & Zwieniecki, 2011). In addition, the transcripts encoding
As mentioned previously, AQP in vivo localization studies PIP1.1 and PIP1.3 were the most expressed among PIP
aquaporin genes in poplar stems (Secchi et al., 2009). These two woody plants remains incomplete. General agreement exists
genes were highly up-regulated in response to artificially- that the living parenchyma cells associated with xylem conduits
induced embolism, and their expression was repressed when are involved in the recovery process from stress. They are
plants recovered from embolism, showing VACs ability to credited with supplying water to fill the void and releasing os-
sense both embolism formation and end of the refilling process motically active compounds to generate energy gradients
(Secchi & Zwieniecki, 2010). Similarly, a Vitis PIP1;1 gene was needed to pull water from living cells and restore hydraulic
reported to be activated in VACs during both embolism forma- function (Nardini et al., 2011a, Salleo et al., 2004, Zwieniecki
tion and recovery, whereas the same transcript was not de- & Holbrook, 2009). Thus, we can postulate that a correlation
tected at the whole tissue level (Chitarra et al., 2014, Perrone between a plant’s capacity to recover from severe drought
et al., 2012b, see also Table 1). These findings demonstrate that and VAC volume, surface area or bridges provided between
PIP1 expression is affected by drought stress, embolism and du- phloem and xylem should also exist. If so, more detailed ana-
ration of recovery from stress. However, hypotheses about tomical studies of xylem parenchyma in combination with spe-
PIP1s role in refilling remain open as all evidence is based on cies drought tolerance may lead to of the discovery of
transcription analyses, and no direct proof exists on the physio- interesting patterns linking drought tolerance and parenchyma
logical activity of these proteins. activity evolution. As xylem refilling process might require wa-
Reverse genetic techniques have successfully been applied ter transport from living cells to xylem lumens, reductions of
to the functional characterization of AQP genes mainly in her- membrane hydraulic resistance would be beneficial during re-
baceous species (Aharon et al., 2003, Da Ines et al., 2010, covery from stress and thus observing patterns of expression
Kaldenhoff et al., 1998, Martre et al., 2002, Postaire et al., and activity of specific AQP isoforms in living parenchyma cells
2010) and more recently in woody plants (Bi et al., 2015, might provide further clues to biology of stem under drought
Perrone et al., 2012a, Secchi & Zwieniecki, 2013, Sreedharan conditions. So far, only a handful of species have been studied,
et al., 2013, Tsuchihira et al., 2010). A similar reverse genetic ap- and we can neither address the question of how common de-
proach was used to generate transgenic poplar lines by down- scribed expression patterns are among species, nor provide a
regulating the whole PIP1 gene family, with the goal of comprehensive overview of specific PIPs involved in the recov-
attesting the function of this PIP group by gaining in vivo evi- ery process.
dence of their role during xylem embolism and recovery Another important aspect of plant recovery from severe wa-
(Secchi & Zwieniecki, 2014). The down-regulation of PIP1s ter stress that includes the restoration of xylem hydraulic ca-
did not affect plant behaviour under well-watered conditions pacity is related to signalling (triggers) for the biological
(Secchi & Zwieniecki, 2013), but it changed the physiological responses of VACs. Although we can observe changes in
response of poplar during the progression of water stress. Spe- VAC physiological and expression activity, we do not know
cifically, the suppression of PIP1 expression activity signifi- what physical or chemical changes trigger these responses. Sev-
cantly lowered refilling activity, resulting in an apparent eral ideas have been suggested like mechano-sensing of high
increase in the vulnerability to embolism formation of trans- frequency sound waves associated with embolism (Salleo
genic plants (Secchi & Zwieniecki, 2014). These findings have et al., 2008), changes in sucrose concentration in the xylem
clearly elucidated that, under water stress, the function of stem apoplast (Nardini et al., 2011a, Secchi & Zwieniecki, 2011) or
PIP1s is pivotal to both the maintenance of xylem transport ca- changes in pH (Secchi & Zwieniecki, 2016). In this review’s
pacity under stress and plant recovery from stress. model (Fig. 1), sucrose concentration is the proposed trigger
In conifers, the occurrence of freeze-thaw induced embolism for embolism repair processes as previous results suggest that
formation and recovery processes is also documented (Limm increased sucrose concentration in the xylem follows an ex-
et al., 2009, Mayr et al., 2006, Mayr et al., 2002, Sparks & Black, pression pattern similar to that of VAC gene expression in re-
2000, Sparks et al., 2001), but to date, very few research reports sponse to the formation of embolism (Secchi & Zwieniecki,
have provided experimental evidence that these phenomena 2011). A more recent work also suggests that xylem apoplastic
can affect AQP gene regulation. In P. abies, frost-induced em- pH may be a significant part of the signalling path responsible
bolism has been shown to significantly correlate with the accu- for refilling apart from its role in invertase activity and sugar ac-
mulation of PIP1 and PIP2-type proteins in needle endodermal cumulation (Secchi & Zwieniecki, 2016). Low pH was shown to
and phloem cells (Mayr et al., 2014). In P. glauca, AQPs were affect aquaporin molecular gating (Maurel et al., 2015,
shown to promote xylem refilling by facilitating water move- Tornroth-Horsefield et al., 2006, Tournaire-Roux et al., 2003),
ment between VACs and the embolized xylem (Laur & Hacke, which depends on protonation of the conserved amino acid res-
2014). Although more experimental efforts are needed to idue of loop D (His193 in SoPIP2;1). At acidic pH, charged hy-
deepen existing knowledge of conifer AQP roles in recovery drogen interacts with two additional amino acids (Asp28 and
from embolism, the findings described previously provide some Glu31) and loop B (Ser115) to stabilize loop D in a closed pore
indication that gymnosperms are capable of sensing and man- conformation (Tornroth-Horsefield et al., 2006). This activity
aging xylem embolism. has been observed in heterologous systems (Xenopus oocytes)
or in herbaceous species (spinach and Arabidopsis) (Tornroth-
Horsefield et al., 2006, Tournaire-Roux et al., 2003). Because
FUTURE DIRECTIONS
xylem apoplastic pH triggers multiple parts of the recovery
Despite research efforts, our understanding of the biophysical process (i.e. membrane sucrose transport, AQP gating and
and cellular mechanisms responsible for embolism refilling in the activity of apoplastic invertase), it is crucial to study the
in vivo chemistry of xylem and VACs following a whole system Carpaneto A., Koepsell H., Bamberg E., Hedrich R. & Geiger D. (2010) Sucrose-
and H+-dependent charge movements associated with the gating of sucrose
approach. transporter ZmSUT1. Plos One 5, DOI: 10.1371/journal.pone.0012605.
Chapotin S.M., Razanameharizak J.H. & Holbrook N.M. (2006) Abiomechanical
perspective on the role of large stem volume and high water content in baobab
trees (Adansonia spp.; Bombacaceae). American Journal of Botany 93,
ACKNOWLEDGEMENTS 1251–1264.
Chitarra W., Balestrini R., Vitali M., Pagliarani C., Perrone I., Schubert A. &
We would like to thank Jessica Orozco, Anna Davidson and Lovisolo C. (2014) Gene expression in vessel-associated cells upon xylem em-
Jessie Godfrey for their comments and editorial help. F. S. ac- bolism repair in Vitis vinifera L. petioles. Planta 239, 887–899.
Choat B., Cobb A.R. & Jansen S. (2008) Structure and function of bordered pits:
knowledges funding from the ‘Programma Giovani Ricercatori
new discoveries and impacts on whole-plant hydraulic function. New
Rita Levi Montalcini’s’ grant. Phytologist 177, 608–625.
Choat B., Brodersen C.R. & McElrone A.J. (2015) Synchrotron X-ray
microtomography of xylem embolism in Sequoia sempervirens saplings during
cycles of drought and recovery. New Phytologist 205, 1095–1105.
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Plant, Cell and Environment (2017) 40, 858–871 doi: 10.1111/pce.

The functional role of xylem parenchyma cells and aquaporins

ABSTRACT hydraulic conductivity. In recent years, signiﬁcant efforts have

Gene ID NCBI Response to

Gene ID NCBI Response to

PgPIP2;7 P. glauca BT106222 (a) R, S (Laur & Hacke, 2014)

Gene ID NCBI Response to

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