Living to die and dying to live: The survival strategy behind leaf senescence

46 Pages·2015·1.21 MB·English

Plant Physiology Preview. Published on August 14, 2015, as DOI:10.1104/pp.15.00498
1 Running head: The survival strategy behind leaf senescence
2
3 Corresponding authors:
4
5 Jos Schippers,
6
7 Institute of Biology I, RWTH Aachen University, Worringerweg 1, 52074 Aachen, Germany.
8
9 Email:
19 Title:
20
21 Living to die and dying to live: The survival strategy behind leaf senescence
22
1, 1, 2 3
23 Jos H.M. Schippers * , Romy Schmidt *, Carol Wagstaff , Hai-Chun Jing
24
25
1
26 Institute of Biology I, RWTH Aachen University, Worringerweg 1, 52074 Aachen, Germany.
27
2
28 Department of Food and Nutritional Sciences, University of Reading, Whiteknights Campus,
29 PO Box 226, Reading, Berkshire, RG6 6AP, UK.
30
3
31 The Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences,
32 Beijing 100093, China.
33
34 * These authors contributed equally to this work.
35
36 Summary
37 Leaf senescence is a highly dynamic process that has a major impact on crop production
38 and quality.
39
2

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
40 Financial source:
41
42 The work was supported by RWTH Aachen University to JHMS and RS, Natural Science
43 Foundation of China to HCJ (grant numbers 30970252 and 31471570).
44
45 Corresponding authors with e-mail address:
46
47 Jos Schippers
48
49
56 Abstract
57 Senescence represents the final developmental act of the leaf, during which the leaf cell is
58 dismantled in a coordinated manner to remobilize nutrients and to secure reproductive
59 success. The process of senescence provides the plant with phenotypic plasticity to help it
60 adapt to adverse environmental conditions. Here, we provide a comprehensive overview of
61 the factors and mechanisms that control the onset of senescence. We explain how the
62 competence to senesce is established during leaf development, as depicted by the
63 senescence window model. We also discuss the mechanisms by which phytohormones and
64 environmental stresses control senescence, as well as the impact of source-sink
65 relationships on plant yield and stress tolerance. In addition, we discuss the role of
66 senescence as a strategy for stress adaptation and how crop production and food quality
67 could benefit from engineering or breeding crops with altered onset of senescence.
4

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
68 Introduction
69 It does not take an expert’s eye to notice how plant senescence is manifested in our daily
70 lives. Senescence limits the shelf life of fresh vegetables, fruits and flowers, implying that it is
71 detrimental to survival. However, from the plant's perspective, senescence supports plant
72 growth, differentiation, adaptation, survival and reproduction (Thomas, 2013). Senescence is
73 under strict genetic control, which is crucial for the plant’s nutrient use efficiency and
74 reproductive success. Senescence represents a major agricultural trait that affects crop yield
75 and grain quality during food and feed production.
76 During senescence, mesophyll cells are dismantled in a programmed manner,
77 undergoing changes in cell structure, metabolism and gene expression. Ultra-structural
78 studies have shown that chloroplasts are the first organelles to be dismantled (Dodge, 1970),
79 while mitochondria and the nucleus remain intact until the final stages of leaf senescence
80 (Butler, 1967). The salvaging of the chloroplasts allows a major portion of leaf lipids and
81 proteins to be recycled (Ischebeck et al., 2006). As chloroplasts contain the majority of leaf
82 proteins, they represent a rich source of nitrogen, and their salvaging provides up to 80% of
83 the final nitrogen content of grains (Girondé et al., 2015).
84 During senescence, autotrophic carbon metabolism of the leaf is replaced by
85 catabolism of cellular organelles and macromolecules. Metabolic profiling studies have
86 revealed that N-containing and branched chain amino acids accumulate in senescing leaves
87 (Masclaux et al., 2000; Schippers et al., 2008). Interestingly, plants undergoing carbohydrate
88 limitation metabolize proteins as alternative respiratory substrates (Araújo et al., 2011). Thus,
89 to some extent, the availability of free amino acids ensures the maintenance of energy
90 homeostasis in the senescing leaf, while these amino acids are also transported to sink
91 tissues such as grains to support protein synthesis and N storage.
92 In addition to N remobilization, senescing leaves also undergo extensive lipid
93 turnover. In both monocot and dicot plants, the total fatty acid content of senescing leaves
94 decreases by at least 80% (Yang and Ohlrogge, 2009). Upon senescence, lipid synthesis
95 rates are reduced, while the peroxisomal β-oxidation pathway is up-regulated (Christiansen
96 and Gregersen, 2014). In Arabidopsis (Arabidopsis thaliana), remobilization of chloroplast
97 lipids is essential for normal plant growth, the onset of senescence and reproductive success
98 (Padham et al., 2007).
99 Phosphate is a major component of plant fertilizers used in high-yield agriculture. In
100 general, soil phosphate levels are suboptimal. Therefore, plants have evolved efficient
101 mechanisms to remobilize stored phosphate during senescence (Himelblau and Amasino,
102 2001). Phosphate is remobilized through the degradation of organellar DNA and RNA, as
103 well as cytosolic ribosomal RNA. As decreased phosphate remobilization reduces total
104 phosphate levels in seeds, as well as seed germination rates (Robinson et al., 2012),
5

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
105 senescence is crucial for seed viability. Furthermore, micronutrients such as Zn, Fe and Mo
106 are strongly redistributed during senescence (Himelblau and Amasino, 2001). In wheat
107 (Triticum turgidum), the senescence-associated NAC transcription factor Gpc-B1 positively
108 regulates the onset of leaf senescence, as well as the translocation of Zn and Fe to grains
109 (Uauy et al. 2006). Also, the transition metal Mo, an essential cofactor of enzymes involved
110 in nitrogen assimilation, sulfite detoxification and phytohormone biosynthesis, is readily
111 remobilized upon senescence (Bittner, 2014).
112 Considering the investment of plants in nutrient acquisition, remobilization of macro-
113 and micronutrients during senescence is critical for efficient nutrient usage and for plant
114 survival. The onset of senescence is strictly regulated and occurs under optimal conditions in
115 an age-dependent manner (Figure 1). However, upon exposure to environmental stress or
116 nutrient deficiency, the plant can execute the senescence program as an adaptive response
117 to promote survival and reproduction.
118 In this review, we address the role of senescence as an adaptive strategy to help the
119 plant respond to its fluctuating environment, and we also discuss the extent to which
120 manipulating this process would be beneficial to agriculture. First, we focus on internal and
121 external factors that determine the onset of senescence, and we highlight the importance of
122 the senescence process during plant adaptation to environmental stress. Next, we discuss
123 sink-source relations and the adaptive advantage of senescence for plant survival in the field.
124 Finally, we explore the role of senescence in regulating crop yield and grain quality and its
125 implications for agriculture.
126
127 Onset of leaf senescence
128 Under optimal growth conditions, the onset of leaf senescence occurs in an age-dependent
129 manner (Schippers et al., 2007). Leaf senescence involves a complex interplay between
130 internal and external factors, which determine the timing, progression and completion of
131 senescence. The model plant species Arabidopsis exhibits two types of senescence:
132 sequential and reproductive senescence. During sequential senescence, older leaves
133 senesce and their nutrients are translocated to younger, growing parts of the plant. This type
134 of senescence is independent of reproduction, since male and female sterility increase plant
135 longevity, while the lifespan of individual leaves remains unaffected (Noodén and Penney,
136 2001). Reproductive senescence occurs at the whole-plant level in monocarpic plants
137 (Figure 1) and promotes seed viability and quality. First, we will introduce the concept of
138 developmental senescence and the senescence window. We will then provide a concise
139 overview of the role of plant hormones in the timing and progression of senescence.
140
141 Developmental senescence and the senescence window concept
6

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
142 The identification of molecular markers for leaf senescence was a great breakthrough, which
143 paved the way for elucidating leaf senescence at the transcriptional level. For instance, age-
144 dependent induction of senescence in leaves by ethylene was first demonstrated using
145 SENESCENCE ASSOCIATED GENE 2 (SAG2) and SAG12 as molecular markers (Grbić
146 and Bleecker, 1995). The relationship between leaf age and ethylene-induced senescence
147 was studied in detail by Jing et al. (2002), resulting in the concept of the senescence window
148 (Figure 2). Over time, the senescence window concept was extended and used to explain
149 how the onset of senescence relies on the integration of hormones or external factors into
7

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
150 leaf ageing (Schippers et al., 2007). The window concept assumes three distinct leaf
151 developmental phases in relation to the induction of senescence. The first phase
152 corresponds to early development (growth) and is a ‘‘never senescence phase’’. Leaves,
153 which arise as heterotrophic cell outgrowths from the shoot apical meristem (SAM), act as
154 sink tissues during their early phase of development. During the phase of proliferation and
155 expansion, the leaf responds differently to senescence-inducing factors (Graham et al.,
156 2012). For instance, ethylene application to growing leaves does not induce senescence,
157 instead resulting in reduced cell proliferation and expansion (Skirycz et al., 2010). In other
158 words, the strategy of the plant is to protect young tissues from precocious senescence.
8

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
159 Maturation of the leaf represents the second phase of the senescence window concept,
160 during which the leaf becomes competent for internal and external factors to activate
161 senescence (Figure 2). The effect of senescence-inducing factors at this stage increases
162 with leaf age, indicating that the leaf becomes more competent to undergo senescence. In an
163 attempt to explain this observation, the term age-related changes (ARCs) was introduced
164 (Jing et al., 2005; Schippers et al., 2007). During leaf development, these ARCs accumulate
165 to a level under which senescence will be induced even under optimal growth conditions, as
166 illustrated by the final phase of the senescence window concept (Figure 2). However,
167 although leaves become more permissive to the induction of senescence with age, they
168 remain competent for perceiving senescence-delaying or -reverting signals (Gan and
169 Amasino, 1995), indicating that the accumulation of ARCs does not affect the vigor of the
170 leaf.
171
172 Ethylene
173 Ethylene induces a senescence program that has physiological, biochemical and genetic
174 features of developmental leaf senescence. Mutating ethylene signaling or biosynthesis
175 genes affects the timing of senescence (Graham et al., 2012; Bennet et al., 2014). For
176 instance, the ethylene-insensitive mutants ethylene receptor 1-1 (etr1-1) and ethylene
177 insensitive 2 (ein2) exhibit delayed senescence (Grbić and Bleecker, 1995; Alonso et al.,
178 1999), while overexpressing the transcription factor gene EIN3 causes early leaf senescence
179 (Li et al., 2013). Ethylene signaling relies on the nuclear translocation of EIN2 and the
180 subsequent activation of two transcription factors, EIN3 and EIN3-LIKE 1 (EIL1; Chang et al.,
181 2013). Recently, an extensive genome-wide chromatin immunoprecipitation assay for EIN3
182 was performed, covering seven time-points after ethylene treatment (Chang et al., 2013),
183 which resulted in the identification of 1,314 candidate target genes of EIN3. Considering the
184 role of ethylene in senescence, we compared the target list with genes known to be induced
185 during senescence (Guo et al. 2004; Buchanan-Wollaston et al. 2005), finding that 269 SAGs
186 are among the reported EIN3 targets (Figure 3A; Supplemental Table 1), which we refer to
187 as EIN3-Bound SAGs (EB-SAGs). The study by Chang et al. (2013) was performed on
188 seedlings, which (according to the senescence window) are in the never-senescence phase.
189 Indeed, this simultaneous expression profiling revealed that only 76 of the 269 EB-SAGs are
190 responsive to ethylene at the seedling stage. Thus, binding of EIN3 to an EB-SAG promoter
191 is, in most cases, not sufficient to activate the senescence program, suggesting that an
192 additional component is required.
193 As ethylene induces senescence in many plant species, we examined whether the
194 transcriptional network downstream of EIN3 is conserved. To this end, we performed bi-
195 directional BLAST searches with the Arabidopsis EB-SAGs against the rice (Oryza sativa)
9

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.
196 genome using the Phytozome database (Goodstein et al., 2012). Interestingly, we found rice
197 homologues for 159 Arabidopsis EB-SAGs, and in more than 90% of the cases, at least one
198 EIN3 core binding site (TACAT) was found in the upstream promoter regions (Supplemental
199 Table 1). These findings suggest that ethylene controls similar processes during senescence
200 in Arabidopsis and rice. Gene ontology analysis (Proost et al., 2009) further revealed a
201 significant enrichment for terms related to catalytic activity, transcription and transport
202 (Figure 3B), which is in line with previous reports demonstrating that ethylene is required for
203 nutrient remobilization during senescence (Jung et al., 2009).
204
205 Cytokinin
206 Richmond and Lang (1957) reported that cytokinin (CK) delays the onset of senescence by
207 preventing chloroplast breakdown. The senescence-delaying feature of CK is commonly
208 used by pathogens and herbivores to establish so-called green islands (Walters et al., 2008).
209 By placing a CK biosynthesis gene encoding an isopentenyl transferase under the control of
210 the SAG12 promoter, it is possible to retard developmentally induced senescence (Gan and
211 Amasino, 1995). In addition, drought-induced senescence can be prevented by placing the
212 IPT gene under a stress- and maturation-induced promoter (Rivero et al., 2007). The
213 mechanisms behind CK-delayed senescence mainly involve metabolic reprogramming that
214 assigns a sink signature to the organ. CK treatment results in the coordinated induction of an
215 extracellular invertase (CIN1) and hexose transporter genes, leading to higher uptake of
216 hexoses (Ehneß and Roitsch 1997). Invertases mediate the hydrolytic cleavage of sucrose
217 into hexose monomers at the site of phloem unloading, and metabolization of these cleavage
218 products controls the sink strength (Roitsch and González, 2004). Interestingly, in plants with
219 reduced extracellular invertase activity, CK fails to delay senescence (Balibrea Lara et al.,
10

Downloaded from on December 27, 2018 - Published by www.plantphysiol.org
Copyright © 2015 American Society of Plant Biologists. All rights reserved.