# Plant senescence: how plants know when and how to die

Hye Ryun Woo, Céline Masclaux-Daubresse, Pyung Ok Lim

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Hye Ryun Woo, Céline Masclaux-Daubresse, Pyung Ok Lim. Plant senescence: how plants know when and how to die. Journal of Experimental Botany, 2018, 69 (4), pp.715-718. 10.1093/jxb/ery011 . hal-02626345

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Plant senescence: how plants know when and how to die

Virtually all of the cells, tissues and organs in plants age, senesce and eventually die. Senescence is regarded as an evolutionarily acquired process that is critical for plant fitness, and understanding its detailed molecular nature is not only fundamental but also pivotal for the improvement of crop yield and postharvest storage. Impressive progress has been made in revealing new molecular regulatory mechanisms in recent years. In this special issue, reviews span this emerging knowledge - derived from unique biological processes in different types of plant senescence - and highlight key molecular pathways and network-based regulatory mechanisms, as well as their evolutionary implications. The issue also addresses future research perspectives, including new technologies and approaches.

Plant senescence defines the last stage of a developmental program, which is a degenerative process, but occurs in a temporally coordinated manner (Gan and Amasino, 1997; Lim et al., 2007). It has long been considered as an evolutionarily acquired strategy that is tightly associated with reproduction and survival. During the senescence process, plants integrate multiple internal and external signals as well as information about developmental age through intricate regulatory pathways (Thomas and Stoddart, 1980; Buchanan-Wollaston et al., 2003; Lim et al., 2007). Such integrated characteristics provide the individual with optimal fitness in a given ecological position by regulating the timing of initiation, rate of progression and nature of senescence. Despite its biological importance, however, many molecular mechanisms underlying plant senescence are still largely unknown due to their extreme complexity.

A fundamental question in the field, as yet unanswered, is how plants 'know' when and how to die. Six major research themes which address this and constitute the basis of this special issue include (1) changes in the photosynthetic apparatus during leaf senescence, (2) the interaction of endogenous and exogenous signals with senescence pathways, (3) integrative, multi-layered, spatio-temporal networks in leaf senescence, (4) the evolutionary basis of leaf senescence, (5) extended applications of multi-omics technologies to explore genetic elements and their networks that control plant senescence, and integration of multiple types of omics and genetic/physiological data, and (6) source-sink interactions for enhancing crop yield. Although the majority of the reviews focus on leaf senescence, Ma et al. (2018) discuss recent progress in understanding hormone-regulated petal senescence; and Patharkar and Walker (2018) address recent advances in understanding the abscission signalling network, as well as future directions for the application of basic abscission research to agriculture.

Changes in the chloroplasts during plant
senescence

During senescence, leaf cells are subject to massive physio-
logical and biochemical changes, including a dramatic meta-
bolic transition from anabolism to catabolism which results
in nutrient redistribution to newly developing organs (Lim
et al., 2007). The transition from carbon assimilation to nutri-
ent remobilization involves the degradation of cellular struc-
tures such as chloroplasts (Masclaux et al., 2000). Two reviews
in this issue deal with changes in the chloroplasts, reflecting
the rapid progress of research in this area. Chloroplast deg-
radation is co-ordinately regulated by both intra-plastidic
and extra-plastidic degradative pathways (Martinez et al.,
2008). Otegui (2018) considers the extra-plastidic processes,
reviewing how plant cells degrade chloroplast components
in vacuoles through autophagy-dependent and -independent
trafficking mechanisms. Chlorophyll in chloroplasts is also
massively degraded, which results in leaf yellowing, one of
the most obvious visible signs of plant senescence (Ougham
et al., 2005). Kuai et al. (2018) discuss the multi-step, pheo-
phorbide a oxygenase/phyllobilin pathway for chlorophyll
breakdown particularly focusing on biochemical and molecu-
lar understanding, evolutionary aspects and the transcrip-
tional regulation of the pathway. In addition, Guyer et al.
(2018) explore the biochemical and structural properties of
Arabidopsis pheophytinase (PPH), a key enzyme associated
with chlorophyll degradation. The amino acid residues that
form the catalytic triad of PPH are also identified through
*in silico* modelling of the 3D structure combined with site-
directed mutagenesis (Guyer et al., 2018).

Regulatory mechanisms underlying leaf
senescence

The leaf senescence research field has massively enlarged and
made great advances over the past couple of decades, but the
methods for physiological and molecular investigations are
still diverse. In this special issue, Bresson et al. (2018) attempt
to provide standardized guidelines for leaf senescence anal-
yses in Arabidopsis, including an experimental design for
measuring senescence phenotypes at physiological, biochem-
ical and molecular levels.

Recent molecular genetic studies as well as omics analyses
of leaf senescence have enormously expanded our knowledge
of the underlying molecular mechanisms (Woo et al., 2013;
Kim et al., 2016). Kim et al. (2018) review recent advances
in this area, particularly aspects of dynamic regulation and
**Box 1. A systems understanding of how a plant knows when and how to die**

Plant senescence constitutes a part of the overall developmental program, in which multiple internal and external signals are integrated into information about developmental age through intricate regulatory pathways. Given the multifaceted nature of the senescence process in plants, integrative analyses which allow an assessment of the dynamic changes that occur in physiological, biochemical and molecular phenotypes is required for a systems understanding of its underlying mechanistic principles. Different multi-omics datasets, such as genomics, epigenomics, transcriptomics, proteomics, metabolomics and phenomics, are integrated for systems biology approaches, and these should provide a more accurate picture of the regulatory networks underlying plant senescence.

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coordination at multiple levels. Their review also emphasizes the necessity of understanding leaf senescence as a life history strategy from the perspective of system-level spatio-temporal changes and evolution. In addition, recent findings have shed light on the molecular basis of epigenetic and post-transcriptional regulation of leaf senescence (reviewed by Yolcu et al., 2018). As highlighted by Yolcu et al. (2018), epigenetic regulation, including chromatin remodelling and modification of DNA, histones and small RNA function, is another key mechanism for modulating gene expression during leaf senescence.

One of the most exciting advances in understanding the regulatory mechanisms of leaf senescence is the identification of diverse transcription factors that play critical roles in the process. Kim et al. (2018) highlight the way that dynamic activation and/or deactivation of transcription factors is a key mechanism that controls genome-wide transcriptome

changes by continuously integrating developmental and environmental signals. Intriguingly, in this special issue Li et al. (2018) address the potential roles of genetic redundancy in senescence-associated transcription factors in the leaf senescence program by analyzing the relationships between gene duplication, gene expression level and phenotypic variation in leaf senescence.

Given that senescence in plants is a highly dynamic process that is precisely coordinated by a complex regulatory network in response to endogenous developmental signals and environmental cues, investigations of leaf senescence should be accomplished by integrative analyses which allow an assessment of the spatio-temporal, dynamic changes that occur in physiological, biochemical and molecular phenotypes. Großkinsky et al. (2018) point out the importance of a phenomics approach integrated with multi-omic techniques in senescence research for a better understanding of the process as a complex system.
Prospects for crop improvement

Leaf senescence is a very important trait for agronomic plants as it limits yield and biomass and modifies nutritional value. For that reason, interest in its manipulation in plant breeding programmes has promoted research projects dedicated to identifying the molecular mechanisms involved in the process, including regulation. The best known biotech application of leaf senescence manipulation technology for plant productivity and quality is the strategy of promoting cytokinin synthesis in senescing leaves by overexpressing *IPT* under the control of senescence-associated promoters (Guo and Gan, 2014). In addition to enhancing grain yield and biomass in many crops, these constructs enhance tolerance to drought stress. In this special issue, Sade *et al.* (2018b) show that the down-regulation of *OsCV* expression in rice contributes to water-deficit stress tolerance. *OsCV*, which is involved in chloroplast vesiculation, contributes to chloroplast degradation and is enhanced in ageing leaves and by drought. Silencing *OsCV* contributes to the maintenance of chloroplast integrity and maintains carbon fixation and primary nitrogen assimilation. In their review, Sade *et al.* (2018a) show that many transcription factors that play a role in the control of age-induced leaf senescence also play a role in plant stress tolerance. The common feature of age-induced and stress-induced leaf senescence is chloroplast breakdown, and the authors report that many *STAYGREEN (SGR)* genes have been shown to play significant roles in regulating chlorophyll breakdown under ‘natural’ and both abiotic and biotic stress-induced senescence. Sade *et al.* (2018a) provide a comprehensive overview of the common features regulating source-sink relationships, nutrient recycling and crop performance under age-dependent and stress-induced senescence. They also discuss the role of leaf senescence in perennial plants for different resource management strategies compared with those in annual plants. The review by Yang and Udvardi (2018) focuses on nitrogen management in perennial grasses during leaf senescence, presenting approaches to improve yield, yield stability and nitrogen use efficiency in perennial grasses for forage versus biofuel, including tilling and genome editing. In addition, Großkinsky *et al.* (2018) address the usefulness of a multi-omics approach combined with a phenomics approach in senescence research for agricultural applications. Finally, the metabolomic study presented by Clement *et al.* (2018) shows that leaf senescence programs in leaf veins and leaf lamina tissues of *Brassica napus* present differences that have never been explored before and need a deeper characterization at the molecular level to clarify the nutrient remobilization processes involved in source to sink exchanges.

Conclusions

Plant senescence is regarded as a complex process in which
various environmental signals are integrated into developmen-
tal, age-dependent pathways. Thus, mechanisms should exist
that sense the age of cells, organs and the whole plant as well

as environmental signals, integrate these signals, transduce the
signals, select the appropriate pathways and execute the degen-
eration process. Investigations of the molecular basis underlying
these critical steps have been performed and this will continue
to be an important area of research. It is more challenging,
however, to address how plants coordinate these processes
temporally and spatially during senescence. Determining how
environmental signals are integrated into information about
developmental age will require not only new technologies but
also new approaches that are being utilized in the systems biol-
ogy field (Box 1). This decision process might be better under-
stood through investigating the evolutionary basis of plant
senescence. Central questions also remain as to how plants bal-
ance environmental signals and developmental signals to allow
such a controlled and unique degeneration process. One of the
new technological challenges to address these issues would be
the establishment of a phenome facility and integration of phe-
nomic data with genomic, proteomic and metabolomic data to
interlink the genetic and environmental inputs to plant growth
and development with an understanding of the controlling
mechanisms from birth to death.

Acknowledgements

We thank Jonathan Ingram, David Mansley and Bennett Young for their help in editing this special issue of *Journal of Experimental Botany*, which was produced following the ‘8th International Symposium on Plant Senescence’ in Jeju, South Korea (2016).

Keywords: Chlorophyll, chloroplast, endogenous signals, exogenous signals, leaf senescence, multi-layered regulatory networks, omics, plant senescence, source-sink interaction.

Hye Ryun Woo¹, Céline Masclaux-Daubresse² and
Pyung Ok Lim¹

¹ Department of New Biology, DGIST,
Daegu 42988, Republic of Korea

² INRA-AgroParisTech, Institut Jean-Pierre Bourgin, UMR1318, ERL CNRS 3559, Saclay Plant Sciences, Versailles, France
Correspondence: hrwoo@dgist.ac.kr or celine.masclaux-daubresse@inra.fr or polim@dgist.ac.kr

References

Bresson J, Bieker S, Riester L, Doll J, Zentgraf U. 2018. A guideline for leaf senescence analyses: from quantification to physiological and molecular investigations. Journal of Experimental Botany 69, 769–786.

Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D. 2003. The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnology Journal 1, 3–22.

Clément G, Moison M, Soulay F, Reisdorf-Cren M, Masclaux-Daubresse C. 2018. Metabolomics of laminae and midvein during leaf senescence and source-sink metabolite management in *Brassica napus* L. leaves. Journal of Experimental Botany 69, 891–903.

Gan S, Amasino RM. 1997. Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiology 113, 313–319.
**Großkinsky DK, Jaya Syaifullah S, Roitsch T.** 2018. Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants. *Journal of Experimental Botany* **69**, 825–844.

**Guo Y, Gan SS.** 2014. Translational researches on leaf senescence for enhancing plant productivity and quality. *Journal of Experimental Botany* **65**, 3901–3913.

**Guyer L, Salinger K, Krügel U, Hörtensteiner S.** 2018. Catalytic and structural properties of pheophytinase, the phytol esterase involved in chlorophyll breakdown. *Journal of Experimental Botany* **69**, 879–889.

**Kim J, Kim JH, Lyu JI, Woo HR, Lim PO.** 2018. New insights into the regulation of leaf senescence in Arabidopsis. *Journal of Experimental Botany* **69**, 787–799.

**Kim J, Woo HR, Nam HG.** 2016. Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. *Molecular Plant* **9**, 813–825.

**Kuai B, Chen J, Hörtensteiner S.** 2018. The biochemistry and molecular biology of chlorophyll breakdown. *Journal of Experimental Botany* **69**, 751–767.

**Li Z, Woo HR, Guo H.** 2018. Genetic redundancy of senescence-associated transcription factors in Arabidopsis. *Journal of Experimental Botany* **69**, 811–823.

**Lim PO, Kim HJ, Nam HG.** 2007. Leaf senescence. *Annual Review of Plant Biology* **58**, 115–136.

**Ma N, Ma C, Liu Y, Shahid MO, Wang C, Gao J.** 2018. Petal senescence: past the point of no return. *Journal of Experimental Botany* **69**, 719–732.

**Martinez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ.** 2008. ‘Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves. *The Plant Journal* **56**, 196–206.

**Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B.** 2000. Characterization of the sink/source transition in tobacco (*Nicotiana tabacum* L.) shoots in relation to nitrogen management and leaf senescence. *Planta* **211**, 510–518.

**Otegui MS.** 2018. Vacuolar degradation of chloroplast components: autophagy and beyond. *Journal of Experimental Botany* **69**, 741–750.

**Ougham HJ, Morris P, Thomas H.** 2005. The colors of autumn leaves as symptoms of cellular recycling and defenses against environmental stresses. *Current Topics in Developmental Biology* **66**, 135–160.

**Patharkar OR, Walker JC.** 2018. Advances in abscission signaling. *Journal of Experimental Botany* **69**, 733–740.

**Sade N, Del Mar Rubio Wilhelmi M, Umnajkitikorn K, Blumwald E.** 2018a. Stress-induced senescence and plant tolerance to abiotic stress. *Journal of Experimental Botany* **69**, 845–853.

**Sade N, Umnajkitikorn K, Del Mar Rubio Wilhelmi M, Wright M, Wang S, Blumwald E.** 2018b. Delaying chloroplast turnover increases water-deficit stress tolerance through the enhancement of nitrogen assimilation in rice. *Journal of Experimental Botany* **69**, 867–878.

**Thomas H, Stoddart JL.** 1980. Leaf senescence. *Annual Review of Plant Physiology* **31**, 83–111.

**Woo HR, Kim HJ, Nam HG, Lim PO.** 2013. Plant leaf senescence and death—regulation by multiple layers of control and implications for aging in general. *Journal of Cell Science* **126**, 4823–4833.

**Yang J, Udvari M.** 2018. Senescence and nitrogen use efficiency in perennial grasses for forage and biofuel production. *Journal of Experimental Botany* **69**, 855–865.

**Yolcu S, Li X, Li S, Kim YJ.** 2018. Beyond the genetic code in plant leaf senescence. *Journal of Experimental Botany* **69**, 801–810.