Contribution of Cellular Autolysis to Tissular Functions During Plant

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Contribution of cellular autolysis to tissular functions

Sacha Escamez and Hannele Tuominen

Plant development requires speciﬁc cells to be eliminated in a fulﬁll different biological functions (Figure 1). For exam-

predictable and genetically regulated manner referred to as ple, while pollen cell death seems to be sufﬁcient to

programmed cell death (PCD). However, the target cells do not prevent inbreeding during self-incompatibility response

merely die but they also undergo autolysis to degrade their (reviewed by [5,6]), in xylem vessels it is the autolysis that

cellular corpses. Recent progress in understanding enables efﬁcient transport of the sap (reviewed by [6,7]).

developmental cell elimination suggests that distinct proteins Experimental evidence is also accumulating to support

execute PCD sensu stricto and autolysis. In addition, cell death distinct execution of cell death sensu stricto and autolysis.

alone and cell dismantlement can fulﬁll different functions. In this review we summarize published data on develop-

Hence, it appears biologically meaningful to distinguish mental cell elimination in higher plant. This data is

between the modules of PCD and autolysis during plant presented within a theoretical framework in which cell

development. death and autolysis represent distinct modules, which

Address may help interpreting the data from an evolutionary

Umea˚ Plant Science Centre, Department of Plant Physiology, Umea˚ perspective [8,9]. Consequently, we use the term

University, SE-90187 Umea˚ , Sweden ‘PCD’ solely for the module which prepares and executes

cell death sensu stricto, while the module which prepares

Corresponding author: Tuominen, Hannele ([email protected])

and executes autolysis is referred to as ‘developmental

regulated cell autolysis’ (dRCA).

Current Opinion in Plant Biology 2017, 35:124–130

This review comes from a themed issue on Growth and development Transport of gas and water require protoplast autolysis

Edited by Ji Hoon Ahn and Marcus Schmid and wall lysis

Xylem vessel formation

Vessel cells or tracheary elements (TEs) degrade their

protoplasts and part of their walls, creating structures

http://dx.doi.org/10.1016/j.pbi.2016.11.017

which transport water much faster than could be done

1369-5266/# 2016 The Author(s). Published by Elsevier Ltd. This is an

by living cells [10–12]. Tonoplast rupture is believed to

open access article under the CC BY-NC-ND license (http://creative-

kill the TEs and to trigger complete protoplast lysis by

commons.org/licenses/by-nc-nd/4.0/).

provoking cytoplasmic acidiﬁcation and release of hydro-

lases [6].

Numerous proteases and nucleases are expressed and

stored in various organelles of the TEs until ﬁnal execu-

Introduction tion of dRCA (reviewed by [6]). Four of them have been

genetically characterized, revealing that they all function

The development of multicellular organisms requires

in protoplast autolysis rather than in PCD. Down-regula-

that they be able to rid themselves of certain cells in a

tion of the nuclease ZEN1 (Zinnia endonuclease1) was

cell autonomous, genetically regulated fashion often

shown to retard nuclear degradation, but not PCD or

called ‘programmed cell death’ (PCD [1]). Since ‘cell

protoplast autolysis, in TE-differentiating Zinnia elegans

death’ refers to the irreversible loss of vital cellular

(Zinnia) cell suspensions [13]. Arabidopsis thaliana (Ara-

functions, it is not alone sufﬁcient for cell elimination

bidopsis) knock-out mutants for XYLEM CYSTEINE

but needs to be associated with dismantlement of the

PROTEASE1 and 2 (XCP1 and 2) and for METACAS-

target cell. Cellular dismantlement by a cell’s own

PASE9 (MC9) showed undegraded protoplast remains

enzymes, or ‘autolysis’ [2], is the main mode of cellular

and slower autolysis, respectively, while PCD seemed

lysis in plants because their cell walls usually prevent

unaffected [14,15]. Interestingly, the xcp1, xcp2, xcp1 xcp2

engulfment by other cells. The term ‘PCD’ has often

and mc9 mutants displayed only partial autolysis defects

been used to encompass both cell death and autolysis,

and no obvious water transport defects [14,15], suggesting

mainly because cell death has proven difﬁcult to record

involvement of additional effectors in TE dRCA.

experimentally and is therefore often deduced from post-

mortem features of cellular breakdown [3]. Yet, in theory it

is possible that different molecular machineries execute Lysigenous aerenchyma formation

cell death sensu stricto and cellular breakdown [3,4], as Plants can maintain gas exchange between the parts

supported by cases where cell death and cellular autolysis of their bodies that lay in anoxic conditions and the

Current Opinion in Plant Biology 2017, 35:124–130 www.sciencedirect.com

Developmental regulated cell autolysis Escamez and Tuominen 125

Figure 1

Outer anther cell layers (e.g. middle layer) Transmitting tract Possible lysis for pollen release Cell lysis possibly helping pollen tube progression Tapetum Antipodal cells Cell lysis supplies the developing Cell lysis of unknown function

pollen with exine material and Receptive synergid enables pollen release Cell lysis required for fertilization

Pollen tube

Cell lysis discharges sperm cells

into the ovule for fertilization

Endosperm Cell lysis required for embryo growth

Embryo suspensor Cell lysis possibly supporting embryo development Testa Possible selective cell lysis supporting seed coat formation Nucellus Cell lysis possibly supporting embryo development

Monocarpic senescence Nutrient recycling function of Tracheary elements selective cell lysis Cell lysis enables water Leaf senescence conduction Nutrient recycling function of selective cell lysis

Aleurone Lateral root cap Cell lysis possibly supporting Cell lysis regulates cell number, germination root growth and possibly auxin signaling

Current Opinion in Plant Biology

Functions of developmental occurrences of cell lysis in Arabidopsis thaliana. The dismantlement of certain cell types at the end of their

differentiation is an integral part of plant development. In Arabidopsis, developmental cell lysis has been observed in the cell types presented in

this figure. In specific cell types (bold black) the cell lysis has been linked to particular biological functions which are presented in this review. In

the other degenerating cell types (grey bold-italic), either the specific function of cell lysis remains unclear or its regulation is intricate, involving

developmental and environmental cues. In contrast with other species, there is no aerenchyma formation, no xylem fiber lysis or xylem

parenchyma lysis occurring during Arabidopsis development in greenhouse conditions.

atmosphere by developing different types of aerenchyma onset of PCD in maize and not only during the late event

tissues [16,17]. The lysigenous type of aerenchyma forms of bulk cell wall degradation [21]. Genes for cell wall

by cell degradation [16,17] and likely evolved multiple remodeling enzymes are induced in developing aeren-

times [16]. Protoplast degradation during aerenchyma chyma in maize and rice [22,23]. Proteases are also

formation differs between rice [18] and maize [19], while induced [22,23], including homologs of the Arabidopsis

their bulk cell wall degradation seems similar [20]. Inter- cysteine endopeptidase CEP1 and MC9, but their role

estingly, changes in cell walls are detected already at the remains to be characterized.

www.sciencedirect.com Current Opinion in Plant Biology 2017, 35:124–130

126 Growth and development

Developmental cell autolysis in the control of 2 [42]. However, PT discharge in Arabidopsis always

reproduction occurs into a degenerating synergid [33 ] and it is there-

Tapetum holocrine secretion fore possible that the RS executes PT burst and lysis,

During anther development, the tapetal cell layer which similar to how autolyzing TEs can harm the surrounding

faces the pollen microspores (MSp) degenerates in an cells in vitro [43,44 ]. Indeed, all reported perturbations of

organized [24] and genetically regulated [25–28] fashion synergid-expressed genes which impair RS degeneration

to release cellular contents into the locule of the anther also impair PT discharge [31,32,33 ,35,36,38,40,45]. PT

[24,28]. This holocrine secretion provides the MSp with burst is blocked in a seemingly autonomous fashion in

material for their outer wall layer (exine) and presumably mutants for two pollen-expressed genes, but these

with nutrients, while its failure results in sterility [24,28]. mutants also display impaired RS degeneration

[33 ,37,39], suggesting that PT signaling fails to trigger

Morphologically, the tapetum dRCA contrasts with that RS degeneration which in turn cannot execute PT burst.

of numerous other cell types [29] as tonoplast rupture Finally, the synergids of maize accumulate a pectin

represents a late event in tapetum degeneration [24]. Rice methylesterase inhibitor (ZmPMEI1) and a defensin-like

plants lacking either of the basic helix-loop-helix (bHLH) protein (ZmES4) which can trigger PT burst in vitro

transcription factors ETERNAL TAPETUM 1 (EAT1 [35,46]. It seems therefore likely that PT undergo ‘cell

[25]) or Tapetum Degeneration Retardation (TDR [30]) murder’ and destruction by the degenerating RS rather

fail to undergo tapetum degeneration. TDR can directly than PCD and dRCA.

regulate a cysteine protease (Os CP1) and a cysteine

protease inhibitor (Os c6), both assumed to function in Developmental cell autolysis in the control of growth

executing PCD and/or cell lysis [30]. EAT1 directly and organogenesis

activates the expression of hydrolases, including two Lateral root cap dRCA and root development

aspartate proteases (OsAP25 and OsAP37) which trigger In numerous angiosperms, the root apical meristem is

both cell death and lytic features when ectopically protected by the central columella and the lateral root cap

expressed in plants and in yeast [25]. On the other hand, (LRC), whose differentiation involves PCD and autolysis

the Arabidopsis male sterility1 (ms1) mutant displays tape- [47,48 ,49]. This process is regulated by the Arabidopsis

tal cell death but not autolysis [26], showing that further transcription factor ANAC033/SOMBRERO (SMB).

work is needed to determine if distinct modules execute Knocking out SMB results in delayed cell death as well

tapetal PCD and dRCA. as impaired autolysis of LRC cells [48 ]. As a result, smb

mutants display too many LRC cells and unprocessed

Pollen tube and synergid lysis in fertilization LRC cell corpses far up into the root expansion zone,

Double fertilization requires transport of the sperm cells leading to altered LRC size and root growth [48 ].

by polar elongation of the pollen tube (PT) until meeting Furthermore, smb mutants develop fewer lateral roots

one of two synergid cells inside the ovule [31]. After than wild type due to disruption in the cyclic pattern

meeting the receptive synergid (RS), the PT ruptures to of LRC cell death and cell removal, which normally

discharge the sperm cells [32]. The RS starts degenerat- contributes to positional signaling [50 ].

ing upon PT arrival in Arabidopsis [33 ] or even earlier in

certain species (summarized in [34]). Both PT and RS The terminal events of LRC differentiation consist of a

lysis are crucial because mutants defective for either fail sudden cytoplasmic pH drop, closely followed by loss of

to achieve fertilization [33 ,35–39]. plasma membrane integrity, tonoplast rupture and bulk

autolysis [48 ]. LCR cells express hydrolases such as

Even though the triggering of RS degeneration most MC9 [15] and the nuclease BFN1 [48 ,51], the latter

often relies on the PT, the degeneration itself seems cell playing the same role during LRC autolysis [48 ] as its

autonomous because it is not completed in Arabidopsis Zinnia homolog ZEN1 in TEs [13]. Interestingly, ectopic

and maize lines with altered expression of several differ- expression of SMB triggers differentiation of TE-like

ent synergid-expressed genes despite the presence of a cells outside of the xylem [52]. These results raise a

PT in the ovule [35,36,38,40]. The molecular machinery question whether LRC and xylem cells share the same

of RS degeneration is unknown but, interestingly, the dRCA module, and whether cytoplasmic acidiﬁcation

upstream molecular effectors are conserved between PT precedes tonoplast rupture also in TEs.

reception and the response to fungal invasion, suggesting

possible conservation of the cell death and lysis modules Endosperm dRCA and embryo growth

between RS and cells responding to fungal invasion [41]. In seeds, the embryo is adjacent to the endosperm, which

serves as a nourishing tissue and therefore ultimately

It is currently unclear whether PT death and burst occur degenerates [53]. The endosperm’s most peripheral part,

cell autonomously. Cell autonomy is supported by PT the aleurone, remains alive until germination [6,53,54].

burst in isolated pollen of Arabidopsis plants lacking the Aleurone degeneration in wheat is associated with nuclear

2+ 2+

receptor-like serine-threonine kinases ANXUR1 and localization of a Ca /Mg -dependent nuclease and

Current Opinion in Plant Biology 2017, 35:124–130 www.sciencedirect.com

Developmental regulated cell autolysis Escamez and Tuominen 127

concomitant autolytic features [55,56], suggestive of PCD PASPA3 but instead regulates cell wall remodeling

and dRCA (reviewed by [6]). enzymes responsible for decreasing the mechanical resis-

tance of the ESR against the growing embryo, which thus

The endosperm ‘embryo-surrounding region’ (ESR) can expand into the ESR space by mechanically pressing

undergoes PCD during seed development [53] but the the endosperm cells to death [58 ]. The lytic enzymes

timing of ESR post-mortem lysis varies between species. involved in ESR dRCA could then be induced either in

While it follows cell death in most angiosperms, bulk lysis response to cell wall modiﬁcations, upon sensing of

is delayed until germination in the starchy endosperm of imminent death from the mechanical pressure, or both.

cereals [53,54]. Starchy endosperm lysis is mainly non-cell

autonomous, requiring enzymes from the scutellar epi- Concluding remarks

thelium [57] and the aleurone [53,54,57]. The ESR Although developmental cell death and cell lysis usually

breakdown of non-cereal species is required for embryo overlap in space and time, recent progress in their mo-

development [58 ] and probably relies on dRCA. In- lecular characterization suggests that they can rely on

deed, induction of the PCD and autolysis markers PU- separate modules, which remain to be fully identiﬁed.

TATIVE ASPARTIC PROTEINASE A3 (PASPA3) and Towards this goal, a bioinformatic survey in Arabidopsis

BFN1 occurs in Arabidopsis and is dependent on the revealed a set of genes that were coregulated in several

ESR-expressed bHLH transcription factor ZHOUPI different tissues undergoing developmental cell death

(ZOU) [58 ]. ZOU does not directly induce BFN1 and and autolysis [59]. Interestingly, PASPA3, BFN1 and

Figure 2

SCW

GFP

proPAS PA3::ToIM (PCD marker) GFP + PI

SCW

GFP

proMC9 ::MC9:GFP (dRCA marker) GFP + PI

SCW

GFP

proIRX1 ::GFP:GUS (SCW biosynthesis marker) GFP + PI

Current Opinion in Plant Biology

Sequential transcriptional activation of PCD and dRCA markers in Arabidopsis TEs. 3D projections of confocal laser scanning micrographs of live

5-days-old Arabidopsis seedlings’ main root, following cell wall staining with propidium iodide (PI; magenta). Translational fusions involving the

green fluorescent protein (GFP; green) were expressed under the transcriptional control of three promoters; proPASPA3, proMC9 and

proIRX1. White arrows and vertical bars marked ‘SCW’ indicate the first PI-stained TE secondary walls. White star indicates root tip. Horizontal

white bars represent 200 mm. TE differentiation progresses from left to right. Transcriptional activation of TE SCW biosynthesis is detected before

visible SCW deposition. Activation of proPASPA3 occurs in TEs without any visible SCW yet while proMC9 activation can only be detected when

TEs already display SCWs.

www.sciencedirect.com Current Opinion in Plant Biology 2017, 35:124–130

128 Growth and development

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