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Escamez, S., Tuominen, H. (2017)
Contribution of cellular autolysis to tissular functions during plant development.
Current opinion in plant biology, 35: 124-130
https://doi.org/10.1016/j.pbi.2016.11.017
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Contribution of cellular autolysis to tissular functions during plant development
Sacha Escamez and Hannele Tuominen
Plant development requires specific cells to be eliminated in a predictable and genetically regulated manner referred to as programmed cell death (PCD). However, the target cells do not merely die but they also undergo autolysis to degrade their cellular corpses. Recent progress in understanding
developmental cell elimination suggests that distinct proteins execute PCD sensu stricto and autolysis. In addition, cell death alone and cell dismantlement can fulfill different functions.
Hence, it appears biologically meaningful to distinguish between the modules of PCD and autolysis during plant development.
Address
Umea˚ Plant Science Centre, Department of Plant Physiology, Umea˚
University, SE-90187 Umea˚, Sweden
Corresponding author: Tuominen, Hannele (hannele.tuominen@umu.se)
Current Opinion in Plant Biology 2017, 35:124–130
This review comes from a themed issue on Growth and development Edited by Ji Hoon Ahn and Marcus Schmid
For a complete overview see theIssueand theEditorial Available online 6th December 2016
http://dx.doi.org/10.1016/j.pbi.2016.11.017
1369-5266/# 2016 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creative- commons.org/licenses/by-nc-nd/4.0/).
Introduction
The development of multicellular organisms requires that they be able to rid themselves of certain cells in a cell autonomous, genetically regulated fashion often called ‘programmed cell death’ (PCD [1]). Since ‘cell death’ refers to the irreversible loss of vital cellular functions, it is not alone sufficient for cell elimination but needs to be associated with dismantlement of the target cell. Cellular dismantlement by a cell’s own enzymes, or ‘autolysis’ [2], is the main mode of cellular lysis in plants because their cell walls usually prevent engulfment by other cells. The term ‘PCD’ has often been used to encompass both cell death and autolysis, mainly because cell death has proven difficult to record 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 cell death sensu stricto and cellular breakdown [3,4], as supported by cases where cell death and cellular autolysis
fulfill different biological functions (Figure 1). For exam- ple, while pollen cell death seems to be sufficient to prevent inbreeding during self-incompatibility response (reviewed by [5,6]), in xylem vessels it is the autolysis that enables efficient transport of the sap (reviewed by [6,7]).
Experimental evidence is also accumulating to support distinct execution of cell death sensu stricto and autolysis.
In this review we summarize published data on develop- mental cell elimination in higher plant. This data is presented within a theoretical framework in which cell death and autolysis represent distinct modules, which may help interpreting the data from an evolutionary perspective [8,9]. Consequently, we use the term
‘PCD’ solely for the module which prepares and executes cell death sensu stricto, while the module which prepares and executes autolysis is referred to as ‘developmental regulated cell autolysis’ (dRCA).
Transport of gas and water require protoplast autolysis and wall lysis
Xylem vessel formation
Vessel cells or tracheary elements (TEs) degrade their protoplasts and part of their walls, creating structures which transport water much faster than could be done by living cells [10–12]. Tonoplast rupture is believed to kill the TEs and to trigger complete protoplast lysis by 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- tion of dRCA (reviewed by [6]). Four of them have been genetically characterized, revealing that they all function in protoplast autolysis rather than in PCD. Down-regula- tion of the nuclease ZEN1 (Zinnia endonuclease1) was shown to retard nuclear degradation, but not PCD or protoplast autolysis, in TE-differentiating Zinnia elegans (Zinnia) cell suspensions [13]. Arabidopsis thaliana (Ara- bidopsis) knock-out mutants for XYLEM CYSTEINE PROTEASE1 and 2 (XCP1 and 2) and for METACAS- PASE9 (MC9) showed undegraded protoplast remains and slower autolysis, respectively, while PCD seemed unaffected [14,15]. Interestingly, the xcp1, xcp2, xcp1 xcp2 and mc9 mutants displayed only partial autolysis defects and no obvious water transport defects [14,15], suggesting involvement of additional effectors in TE dRCA.
Lysigenous aerenchyma formation
Plants can maintain gas exchange between the parts of their bodies that lay in anoxic conditions and the
atmosphere by developing different types of aerenchyma tissues [16,17]. The lysigenous type of aerenchyma forms by cell degradation [16,17] and likely evolved multiple times [16]. Protoplast degradation during aerenchyma formation differs between rice [18] and maize [19], while their bulk cell wall degradation seems similar [20]. Inter- estingly, changes in cell walls are detected already at the
onset of PCD in maize and not only during the late event of bulk cell wall degradation [21]. Genes for cell wall remodeling enzymes are induced in developing aeren- chyma in maize and rice [22,23]. Proteases are also induced [22,23], including homologs of the Arabidopsis cysteine endopeptidase CEP1 and MC9, but their role remains to be characterized.
Developmental regulated cell autolysis Escamez and Tuominen 125
Figure 1
Lateral root cap
Cell lysis regulates cell number, root growth and possibly auxin signaling
Tracheary elements
Cell lysis enables water conduction
Tapetum
Cell lysis supplies the developing pollen with exine material and
enables pollen release Receptive synergid
Cell lysis required for fertilization
Pollen tube
Cell lysis discharges sperm cells into the ovule for fertilization
Endosperm
Cell lysis required for embryo growth Outer anther cell layers
(e.g. middle layer)
Possible lysis for pollen release
Transmitting tract
Cell lysis possibly helping pollen tube progression
Antipodal cells
Cell lysis of unknown function
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 selective cell lysis
Leaf senescence
Nutrient recycling function of selective cell lysis
Aleurone
Cell lysis possibly supporting germination
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.
Developmental cell autolysis in the control of reproduction
Tapetum holocrine secretion
During anther development, the tapetal cell layer which faces the pollen microspores (MSp) degenerates in an organized [24] and genetically regulated [25–28] fashion to release cellular contents into the locule of the anther [24,28]. This holocrine secretion provides the MSp with material for their outer wall layer (exine) and presumably with nutrients, while its failure results in sterility [24,28].
Morphologically, the tapetum dRCA contrasts with that of numerous other cell types [29] as tonoplast rupture represents a late event in tapetum degeneration [24]. Rice plants lacking either of the basic helix-loop-helix (bHLH) transcription factors ETERNAL TAPETUM 1 (EAT1 [25]) or Tapetum Degeneration Retardation (TDR [30]) fail to undergo tapetum degeneration. TDR can directly regulate a cysteine protease (Os CP1) and a cysteine protease inhibitor (Os c6), both assumed to function in executing PCD and/or cell lysis [30]. EAT1 directly activates the expression of hydrolases, including two aspartate proteases (OsAP25 and OsAP37) which trigger both cell death and lytic features when ectopically expressed in plants and in yeast [25]. On the other hand, the Arabidopsis male sterility1 (ms1) mutant displays tape- tal cell death but not autolysis [26], showing that further work is needed to determine if distinct modules execute tapetal PCD and dRCA.
Pollen tube and synergid lysis in fertilization
Double fertilization requires transport of the sperm cells by polar elongation of the pollen tube (PT) until meeting one of two synergid cells inside the ovule [31]. After meeting the receptive synergid (RS), the PT ruptures to discharge the sperm cells [32]. The RS starts degenerat- ing upon PT arrival in Arabidopsis [33] or even earlier in certain species (summarized in [34]). Both PT and RS lysis are crucial because mutants defective for either fail to achieve fertilization [33,35–39].
Even though the triggering of RS degeneration most often relies on the PT, the degeneration itself seems cell autonomous because it is not completed in Arabidopsis and maize lines with altered expression of several differ- ent synergid-expressed genes despite the presence of a PT in the ovule [35,36,38,40]. The molecular machinery of RS degeneration is unknown but, interestingly, the upstream molecular effectors are conserved between PT reception and the response to fungal invasion, suggesting possible conservation of the cell death and lysis modules between RS and cells responding to fungal invasion [41].
It is currently unclear whether PT death and burst occur cell autonomously. Cell autonomy is supported by PT burst in isolated pollen of Arabidopsis plants lacking the receptor-like serine-threonine kinases ANXUR1 and
2 [42]. However, PT discharge in Arabidopsis always occurs into a degenerating synergid [33] and it is there- fore possible that the RS executes PT burst and lysis, similar to how autolyzing TEs can harm the surrounding cells in vitro [43,44]. Indeed, all reported perturbations of synergid-expressed genes which impair RS degeneration also impair PT discharge [31,32,33,35,36,38,40,45]. PT burst is blocked in a seemingly autonomous fashion in mutants for two pollen-expressed genes, but these mutants also display impaired RS degeneration [33,37,39], suggesting that PT signaling fails to trigger RS degeneration which in turn cannot execute PT burst.
Finally, the synergids of maize accumulate a pectin methylesterase inhibitor (ZmPMEI1) and a defensin-like protein (ZmES4) which can trigger PT burst in vitro [35,46]. It seems therefore likely that PT undergo ‘cell murder’ and destruction by the degenerating RS rather than PCD and dRCA.
Developmental cell autolysis in the control of growth and organogenesis
Lateral root cap dRCA and root development
In numerous angiosperms, the root apical meristem is protected by the central columella and the lateral root cap (LRC), whose differentiation involves PCD and autolysis [47,48,49]. This process is regulated by the Arabidopsis transcription factor ANAC033/SOMBRERO (SMB).
Knocking out SMB results in delayed cell death as well as impaired autolysis of LRC cells [48]. As a result, smb mutants display too many LRC cells and unprocessed LRC cell corpses far up into the root expansion zone, leading to altered LRC size and root growth [48].
Furthermore, smb mutants develop fewer lateral roots than wild type due to disruption in the cyclic pattern of LRC cell death and cell removal, which normally contributes to positional signaling [50].
The terminal events of LRC differentiation consist of a sudden cytoplasmic pH drop, closely followed by loss of plasma membrane integrity, tonoplast rupture and bulk autolysis [48]. LCR cells express hydrolases such as MC9 [15] and the nuclease BFN1 [48,51], the latter playing the same role during LRC autolysis [48] as its Zinnia homolog ZEN1 in TEs [13]. Interestingly, ectopic expression of SMB triggers differentiation of TE-like cells outside of the xylem [52]. These results raise a question whether LRC and xylem cells share the same dRCA module, and whether cytoplasmic acidification precedes tonoplast rupture also in TEs.
Endosperm dRCA and embryo growth
In seeds, the embryo is adjacent to the endosperm, which serves as a nourishing tissue and therefore ultimately degenerates [53]. The endosperm’s most peripheral part, the aleurone, remains alive until germination [6,53,54].
Aleurone degeneration in wheat is associated with nuclear localization of a Ca2+/Mg2+-dependent nuclease and
concomitant autolytic features [55,56], suggestive of PCD and dRCA (reviewed by [6]).
The endosperm ‘embryo-surrounding region’ (ESR) undergoes PCD during seed development [53] but the timing of ESR post-mortem lysis varies between species.
While it follows cell death in most angiosperms, bulk lysis is delayed until germination in the starchy endosperm of cereals [53,54]. Starchy endosperm lysis is mainly non-cell autonomous, requiring enzymes from the scutellar epi- thelium [57] and the aleurone [53,54,57]. The ESR breakdown of non-cereal species is required for embryo development [58] and probably relies on dRCA. In- deed, induction of the PCD and autolysis markers PU- TATIVE ASPARTIC PROTEINASE A3 (PASPA3) and BFN1 occurs in Arabidopsis and is dependent on the ESR-expressed bHLH transcription factor ZHOUPI (ZOU) [58]. ZOU does not directly induce BFN1 and
PASPA3 but instead regulates cell wall remodeling enzymes responsible for decreasing the mechanical resis- tance of the ESR against the growing embryo, which thus can expand into the ESR space by mechanically pressing the endosperm cells to death [58]. The lytic enzymes involved in ESR dRCA could then be induced either in response to cell wall modifications, upon sensing of imminent death from the mechanical pressure, or both.
Concluding remarks
Although developmental cell death and cell lysis usually overlap in space and time, recent progress in their mo- lecular characterization suggests that they can rely on separate modules, which remain to be fully identified.
Towards this goal, a bioinformatic survey in Arabidopsis revealed a set of genes that were coregulated in several different tissues undergoing developmental cell death and autolysis [59]. Interestingly, PASPA3, BFN1 and
Developmental regulated cell autolysis Escamez and Tuominen 127
Figure 2
GFP
GFP + PI
SCW
SCW
SCW proPASPA3::ToIM
(PCD marker)
proMC9::MC9:GFP (dRCA marker)
proIRX1::GFP:GUS (SCW biosynthesis marker)
GFP
GFP + PI
GFP + PI GFP
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.
MC9 that were among the most coregulated genes in this study show different temporal expression patterns;
PASPA3 is expressed earlier than BFN1 in the endosperm [58], and earlier than both MC9 (Figure 2) and BFN1 (Escamez and Tuominen, unpublished) in TEs, suggest- ing that PASPA3 might regulate PCD sensu stricto while BFN1 and MC9 are known to be involved in dRCA. It cannot be excluded however that PASPA3 is involved in the early stages of dRCA signaling, and the identity of PCD-specific triggers remains therefore unclear.
Recent work has suggested that cell death sensu stricto may not always require molecular triggers but could be induced by dRCA or mechanical pressure. Yet another non-molecular trigger could be changes in cell wall prop- erties that were recently shown to precede cell death in Arabidopsis seed endosperm [58]. This would also make sense from the evolutionary point of view. PCD and autolysis appeared before multicellularity to increase fitness in phytoplankton populations [60]. Given that the cell wall constitutes a major interface between unicellular plants and their environment, it would not be surprising if cell wall alterations evolved a role in controlling PCD and/or autolysis in unicellular organisms. It remains to be seen whether this function is preserved in higher plants and whether changes in cell wall integrity occur in con- nection to PCD and dRCA also in other cell types than the endosperm.
Acknowledgements
This work was supported by Formas [grant 232-2009-1698];
Vetenskapsra˚det [grant 621-2013-4949], Vinnova (grant 2015-02290), and Bio4Energy funded by the Swedish Government.
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In Arabidopsis, the bHLH transcription factor ZOU controls endosperm degeneration. This study shows that ZOU primarily regulates cell wall modifying enzymes which loosen the walls of the endosperm cells. This Developmental regulated cell autolysis Escamez and Tuominen 129
mechanical weakening is required to allow the growth of the embryo into the space occupied by the endosperm. Furthermore, embryo growth is shown by genetic means to be required for endosperm elimination.
Hence, it seems that the endosperm cells die of mechanical pressure imposed by the growing embryo, followed by cellular autolysis.
59. Olvera-Carrillo Y, Van Bel M, Van Hautegem T, Fendrych M, Huysmans M, Simaskova M, Van Durme M, Buscaill P, Rivas S,
Coll NS et al.: A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants.
Plant Physiol 2015, 169:2684-2699.
60. Bidle KD: The molecular ecophysiology of programmed cell death in marine phytoplankton. Annu Rev Mar Sci 2015, 7:341-375.
