1
Short title: The control of photosynthesis by ethylene 1
Corresponding author 2
Prof. Dr. Ir. Bram Van de Poel 3
Department of Biosystems 4
University of Leuven 5
Willem de Croylaan 42 6
3001 Leuven 7
Belgium 8
0032/16325527 10 11
Update: Ethylene exerts species-specific and age-dependent control of 12
photosynthesis 13
14
Ceusters Johan1,2 & Van de Poel Bram3,* 15
1 KU Leuven, Department of Microbial and Molecular Systems, Bioengineering Technology TC, 16
Campus Geel, Kleinhoefstraat 4, 2440 Geel, Belgium 17 2 UHasselt, Centre for Environmental Sciences, Environmental Biology, Campus Diepenbeek, 18
Agoralaan Building D, 3590, Diepenbeek, Belgium 19 3 KU Leuven, Department of Biosystems, Willem de Croylaan 42, 3001 Leuven, Belgium 20
*corresponding author: [email protected] 21
One sentence summary 22
Ethylene regulates many different aspects of photosynthesis in an age-dependent and species-23
specific manner. 24
Author contributions 25
J.C. and B.V.d.P. performed the literature search and wrote the article. 26
Funding information 27
J.C. and B.V.d.P. thank the Research Fund and Internal Fund of KU Leuven for financial support 28
(OT/14/082, STGBF/16/005 and 3H140277) 29
30
Abstract 31
The volatile plant hormone ethylene plays a regulatory role in many developmental processes and in 32
biotic and abiotic stress responses. One of the under-explored actions of ethylene is its regulation of 33
photosynthesis and associated components such as stomatal conductance, chlorophyll content, light 34
reactions, carboxylation events, carbohydrate partitioning, and age-related senescence. In this 35
update, we summarize the current knowledge concerning the regulation of photosynthesis, focusing 36
on the model species Arabidopsis thaliana. We describe how ethylene directs photosynthesis in 37
juvenile non-senescing leaves and mature senescing leaves. Furthermore, we extend these insights 38
Plant Physiology Preview. Published on February 2, 2018, as DOI:10.1104/pp.17.01706
Copyright 2018 by the American Society of Plant Biologists
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to other types of photosynthesis (C4 and crassulacean acid metabolism) and highlight the species-39
specific effects of the physiological action of ethylene on this complex metabolic pathway. 40
Introduction 41
The volatile plant hormone ethylene (C2H4) is involved in many cellular and developmental 42
processes, such as germination, root and hypocotyl development, climacteric fruit ripening, and 43
senescence (Abeles et al., 1992; Wen et al., 2015; Van de Poel et al., 2015), as well as in the response 44
to biotic and abiotic stress (Bari & Jones, 2009; Kazan et al., 2015). Photosynthesis is one of the least 45
referenced processes regulated by ethylene, which plays a role in all three carbon fixation pathways 46
used by plants: C3, C4, and crassulacean acid metabolism (CAM) (Box 1). Photosynthesis is a complex 47
autotrophic process mediated by the interplay of factors such as light quantity and quality, 48
atmospheric CO2 concentration, stomatal aperture, chlorophyll content, light harvesting complex 49
efficiency, sugar feedback, water availability, nutrient status, and hormonal cues. The role of 50
ethylene in controlling photosynthesis was first described by Kays and Pallas in 1980, who found that 51
the hormone reduces photosynthesis in peanut (Arachis hypogaea). This hormonal control seems to 52
be an ancient response in plants because ethylene downregulates photosynthesis in the charophyte 53
green algae Spirogyra pratensis, suggesting that the regulation of photosynthesis by ethylene is 54
likely conserved and predates the colonization of non-aquatic habits by plants (Ju et al., 2015; Van 55
de Poel et al., 2016). 56
The effect that ethylene exerts on photosynthesis depends on leaf age (Figure 1). Ethylene directly 57
controls photosynthesis in juvenile non-senescing leaves and acts indirectly in mature leaves by 58
promoting leaf senescence. In this review, we describe the effect of ethylene on young non-59
senescing leaves, focusing on the elements that influence plant photosynthesis (chlorophyll content, 60
stomatal conductance, light dissipation, carbon fixation and carbohydrate partitioning). We also 61
briefly highlight the role of ethylene in leaf senescence and refer the reader to a more specialized 62
review on this topic by Kim et al. (2015). 63
64
Ethylene is essential for normal photosynthesis in Arabidopsis thaliana 65
The molecular regulation of photosynthesis by ethylene has been studied using ethylene-related 66
mutants in Arabidopsis and other model plants. Box 2 highlights the steps of the ethylene signaling 67
pathway. Grbic & Bleecker (1998) initially showed that juvenile non-senescing leaves of the 68
Arabidopsis ethylene-insensitive mutant ethylene resistant 1 (etr1-1) possess lower chlorophyll 69
contents, Rubisco activity, and expression of photosynthetically active genes (PAGs) such as CAB 70
(chlorophyll a/b binding protein) and RUBISCO SS (ribulose bisphosphate carboxylase small subunit), 71
suggesting a role for ethylene in controlling photosynthesis in non-senescing leaves. These results 72
were further corroborated by Tholen et al. (2004, 2007, 2008) who showed that ethylene-insensitive 73
mutants of Arabidopsis (etr1-1 and ethylene insensitive 2, ein2) and ethylene-insensitive transgenic 74
tobacco (Nicotiana tabacum) plants carrying the dominant mutant allele of Arabidopsis etr1-1 have a 75
lower whole-plant and leaf photosynthetic capacity, especially under saturating light conditions. 76
These studies suggest that basal ethylene perception is essential for achieving normal 77
photosynthetic capacity in Arabidopsis leaves. In addition, transient ethylene treatment of non-78
senescing leaves reduces chlorophyll content (Zacarias & Reid, 1990) and downregulates CAB 79
expression in Arabidopsis (Grbic & Bleecker, 1995), suggesting that excessive ethylene inhibits 80
photosynthesis in juvenile leaves. To our knowledge, no actual photosynthesis measurements from 81
non-senescing leaves of Arabidopsis exposed to ethylene are currently available. 82
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The control of photosynthesis by ethylene also affects plant biomass production by influencing final 83
rosette size. Arabidopsis ethylene-insensitive mutants (etr1-1, ein2 and ein3) have larger rosettes 84
compared to wild-type plants (Bleecker et al., 1988; Guzman & Ecker, 1990; Ecker et al., 1995; 85
Alonso et al., 1999). However, this discrepancy is probably manifested during later stages of plant 86
development where ethylene controls photosynthesis by stimulating leaf senescence (Figure 1). 87
Ethylene-insensitive mutants show a delayed onset of senescence, extending their growth period, 88
resulting in larger rosettes compared to wild-type plants (Hua et al., 1995; Grbic and Bleecker, 1995; 89
Alonso et al., 1999; Tholen et al., 2004). Juvenile non-senescing 3-week-old etr1-1 mutants grown in 90
well-ventilated conditions do not have a larger total leaf area and relative growth rate compared to 91
wild type plants during vegetative development despite their reduction in photosynthesis, 92
confirming that delayed senescence in these ethylene-insensitive mutants likely controls rosette size 93
(Tholen et al., 2004). 94
95
Ethylene and chlorophyll content 96
Ethylene can stimulate the degradation of chlorophyll during fruit ripening and leaf senescence 97
(Burg & Burg, 1965; Abeles et al., 1992). In non-senescing developing leaves, ethylene-insensitive 98
mutants (e.g. etr1-1) also have reduced chlorophyll content in Arabidopsis, (Zacarias & Reid, 1990; 99
Grbic & Bleecker, 1995) and protoplasts of etr1-1 have reduced chlorophyll fluorescence (Kim et al., 100
2017), suggesting that basal ethylene levels are required to ensure normal chlorophyll content. The 101
opposite is true for mature leaves prone to senescence, where chlorophyll content is found to be 102
higher in ethylene-insensitive mutants (etr1-1 and ein2-1) of Arabidopsis (Grbic & Bleecker, 1995; Oh 103
et al., 1997), tobacco (Yang et al., 2008) and tomato (Solanum lycopersicum) (Monteiro et al., 2011). 104
Chlorophyll content is also higher in mature leaves of ACC oxidase (ACO) antisense lines of tomato 105
(Picton et al., 1993; John et al., 1995; Jensen & Veierskov, 1998) and ACC synthase (ACS) antisense 106
lines of maize (Zea mays) (Young et al., 2002). These findings suggest that ethylene is involved in 107
establishing normal chlorophyll contents in non-senescing leaves and promotes chlorosis through 108
chlorophyll degradation in mature leaves (Figure 1). 109
Ethylene and stomatal conductance 110
Photosynthesis is intimately linked with stomatal conductance, which mediates CO2 uptake and 111
transpiration (Matthews et al., 2017; Vialet-Chabrand et al., 2017; Males & Griffiths, 2017). Ethylene 112
treatment by ethylene gas, ACC, or ethephon induces stomatal closure in Arabidopsis (Desikan et al., 113
2006). The stomata of Arabidopsis ethylene-insensitive mutants (etr1-1) show reduced conductance 114
compared to wild-type plants (Tholen et al., 2004). These observations suggest that ethylene 115
negatively influences stomatal conductance in Arabidopsis. It must be noted that the etr1-1 mutant 116
also has smaller stomata (Tanaka et al., 2005), indicating that ethylene influences stomatal 117
development. Indeed, Arabidopsis plants continuously grown in ethylene, as well as the constitutive 118
ethylene response mutant ctr1-1, possess more stomata (Kieber et al., 1993), yet it is unknown if 119
these plants also display higher CO2 uptake or net photosynthesis. 120
It is not clear if altered ethylene levels play a primary role on stomatal conductance or have a 121
secondary effect through the crosstalk with abscisic acid (ABA) (Wilkinson & Davies, 2010; Murata et 122
al., 2015). In Arabidopsis, external ethylene, or constitutive internal ethylene production by the 123
eto1-1 mutation, inhibits ABA-induced stomatal closure (Tanaka et al., 2005; Watkins et al., 2014). 124
The ethylene signaling mutants (etr1-1 or ein3-1) and the ethylene perception inhibitor 1-MCP (1-125
methylcyclopropane) do not affect ABA-induced stomatal closure (Tanaka et al., 2005). The 126
inhibition of ABA-induced stomatal closure is also observed in wheat (Triticum aestivum), but older 127
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leaves are more sensitive to ethylene, while younger leaves are more sensitive to ABA (Chen et al., 128
2013). The inhibitory action of ethylene on ABA-induced stomatal closure is mainly regulated by 129
hydrogen peroxide signaling (Desikan, 2005; Desikan et al., 2006; Shi et al., 2015). Ethylene 130
stimulates flavonol production in the guard cells, which subsequently suppresses reactive oxygen 131
species (ROS) accumulation and consequently reduces ABA-induced stomatal closure (Figure 1; 132
Watkins et al., 2014; Watkins et al., 2017). 133
Ethylene and energy dissipation (light reactions) 134
The capture of light energy by photosystems (PS) I and II is necessary to accommodate electron 135
transport and the reduction of CO2 (the so-called dark reactions of photosynthesis) in plant 136
chloroplasts. Wullschleger et al. (1992) re-examined the light-response and CO2-response curves of 137
soybean (Glycine max) reported by Taylor and Gunderson (1988) and found a 30% decline in the 138
electron transport capacity (Jmax) following a 4-hour exposure to ethylene. In line with these results, 139
transient overexpression of a specific ethylene responsive factor (CitERF13) in tobacco leaves 140
compromised photosynthetic rates. Significant declines of the maximum quantum efficiency as well 141
as the effective quantum efficiency of both PS I and II occurred respectively 3 and 2 days after 142
infiltration with Agrobacterium carrying CitERF13 (Xie et al., 2016). In addition, pulse-amplitude 143
modulation fluorimetry-based chlorophyll fluorescence analyses by Kim et al. (2017) reveal that 144
ethylene-insensitive mutants of Arabidopsis (etr1-1) display lower PS II activity compared to wild-145
type plants. These results are further corroborated by augmented expression of the cellular energy 146
stress sensor AKIN10 (ARABIDOPSIS KINASE 10) in ethylene-insensitive mutants. AKIN10 is an 147
isoform of the evolutionarily conserved energy sensor SNF1-RELATED PROTEIN KINASE (SnRK1) and 148
has the ability to modulate the ratio catabolism/anabolism to sustain cellular viability (Broeckx et al., 149
2016). It must be noted that a second mutation in the Arabidopsis etr1-1 mutant produces a 150
premature stop codon in ARC3 (ACCUMULATION AND REPLICATION 3), which is responsible for the 151
abnormally large chloroplasts observed in etr1-1 but not ein2 and ein3 mutants (Cho et al., 2012). 152
ARC3 plays a role in chloroplast division (Maple et al., 2007) and the arc3 mutant displays abnormal 153
chloroplasts in mesophyll protoplasts, independent of the etr1-1 mutation (Cho et al., 2012). Given 154
this important secondary mutation (arc3) in the etr1-1 mutant line commonly used in ethylene 155
research, it is advised to seek additional confirmatory lines of evidence, especially when working on 156
photosynthesis. Nonetheless, ethylene signaling mutants outcrossed from the arc3 secondary 157
mutation (etr1-1sg) are also found to have a lower maximum quantum efficiency, higher chlorophyll 158
fluorescence lifetime of PS II and, consequently, a lower quantum yield of PS II (Kim et al., 2017). 159
These findings suggest that normal ethylene sensitivity is required for optimal photochemical 160
efficiency of PS II independently of an altered chloroplast structure caused by the secondary arc3 161
mutation (Kim et al., 2017). Besides photochemical quenching, ethylene has also been found to 162
influence non-photochemical quenching properties by intervention of the xanthophyll cycle 163
mechanism. Chen and Gallie (2015) demonstrated that Arabidopsis eto1-1 mutants, with increased 164
ethylene production, are affected in their ability to convert violaxanthin to zeaxanthin by impairing 165
violaxanthin de-epoxidase activity. As a consequence, these plants are particularly prone to elevated 166
ROS production and photosensitivity. 167
Ethylene and carbon fixation (dark reactions) and carbohydrate partitioning 168
A study by Grbic & Bleecker (1995) showed that young leaves of Arabidopsis ethylene-insensitive 169 mutants (etr1-1) have reduced Rubisco activity, while older leaves have higher rubisco activity 170 compared to wild type plants. Using ethylene-insensitive transgenic tobacco plants, Tholen et al. 171 (2007) also revealed a decrease in Rubisco transcripts and protein content of about 76% and 42%, 172 respectively, in comparison to wild-type plants. A high degree of downregulation of Rubisco occurs 173 for both ethylene-insensitive tobacco and Arabidopsis seedlings growing on a glucose-enriched 174
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medium (Zhou et al., 1998). Further investigations into the decreased rates of photosynthesis in 175 tobacco after transient overexpression of CitERF13 reveal that the maximum rate of Rubisco 176 carboxylase activity (Vc, max) is indeed affected (Xie et al., 2016). We can conclude from these reports 177 that normal ethylene sensitivity is required to achieve maximal Rubisco activity in non-senescing 178 leaves. As Rubisco is inefficient due to its typical error-prone catalytic properties (Bracher et al., 179 2017), ethylene is also likely to influence protein abundance and/or activity of Rubisco activases 180 (RCAs), adding an additional layer of complexity to mediating the carboxylation process. RCAs are 181 well known as molecular chaperones for Rubisco to deal with its dead-end inhibited complexes due 182 to its high affinity for its substrate ribulose 1,5-bisphosphate and similar sugars when the active site 183 has been left unprimed with CO2 and Mg2+ cofactors (Parry et al., 2008). 184 Khan (2005) reported an increased activity of carbonic anhydrase (CA) in mustard (Brassica juncea) 185 upon a treatment with the ethylene-releasing growth regulator ethephon. Besides participating in 186 the regulatory network to control chloroplast pH and protect stroma enzymes from denaturation 187 during severe and sudden changes in light conditions, CA can elevate the concentration of CO2 in 188 close proximity to rubisco and, as such, limit the proportion of photorespiration (Badger, 2003). 189 Carbonic anhydrase also plays a role in C3 but even more critically in C4 and CAM photosynthesis, 190 providing sufficient bicarbonate to fuel PEPC (DiMario et al., 2017). Work on the effect of ethylene 191 on carbon fixation in C4 and CAM plants is limited. Young et al. (2004) reported that an acs6 192 mutation in maize (C4) results in lower ethylene production, leading to higher Rubisco content and 193 higher CO2 assimilation for both young and mature leaves. These results suggest that basal levels of 194 ethylene suppress maximal carbon fixation in maize. We have not found other studies that report 195 the effect of ethylene on Rubisco, CA nor PEPC in other C4 or CAM plants, making it difficult to draw 196 firm conclusions about the impact of ethylene on C4 and CAM carboxylation. 197 Following diurnal synthesis, triose phosphates need to be continuously removed from the Calvin 198
cycle, by either being deployed for starch formation in the chloroplast or exported to the cytosol to 199
fuel sucrose synthesis to replenish non-photosynthetic parts of the plant. Efficient sucrose transport 200
is critical for achieving optimal carbohydrate partitioning in a plant that is robust but also responsive 201
to environmental changes. To carefully monitor the carbohydrate and energy status, plants use an 202
intricate network of transporters, enzymes and metabolites such as sucrose, glucose, triose, and 203
hexose monophosphates, trehalose-6-phosphate, fructose 1,6 bisphosphate, and fructose 2,6 204
bisphosphate (Braun et al., 2014). It is expected that ethylene also intervenes in carbohydrate 205
partitioning, as different nodes have already been established in the complex webs that interrelate 206
sugar and hormone signaling (Figure 1). The mutually antagonistic relationship between glucose and 207
ethylene signaling confers a nice example (Figure 1; Zhou et al., 1998; León and Sheen, 2003). 208
Ethylene-insensitive plants (etr1, ein2 and ein3) are hypersensitive to glucose (supplemented to the 209
medium), while constitutive ethylene activation (ctr1 mutant) or ethylene overproduction (by eto 210
mutants or ACC treatment) result in decreased sugar sensitivity (León and Sheen, 2003; Zhou et al., 211
1998; Yanagisawa et al., 2003). Conversely, glucose also crosstalks with ethylene by stimulating EIN3 212
degradation, which reduces ethylene sensitivity, causing a feedback mechanism that amplifies 213
glucose sensitivity (Yanagisawa et al., 2003). Moreover, in the rubber tree (Hevea brasiliensis), 214
increased latex production after ethylene treatment is accompanied by the enhanced transcript 215
abundance of HbSUT1A and HbSUT2A, which encode transporters belonging to the SUT (sucrose 216
transporter) group (Dusotoit-Coucaud et al., 2009). More recently, Zhou et al. (2017) also reported 217
altered expression of the TREHALOSE-6-PHOSPHATE SYNTHASE genes (HbTPS1 and HbTPS2) upon 218
ethylene treatment in the rubber tree. In addition, ethylene has recently been shown to accelerate 219
the circadian oscillator to shorten the circadian period, a response that can be overturned by 220
externally applied sucrose (Haydon et al., 2017). These findings indicate that ethylene and the pool 221
of sucrose originating from photosynthesis can crosstalk to influence circadian rhythms and control 222
plant photosynthetic capacity (Haydon et al., 2017). 223
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Ethylene and leaf senescence 224
Besides influencing photosynthesis in non-senescing leaves, ethylene also inhibits photosynthesis 225
through the initiation and stimulation of senescence in mature leaves (Figure 1; Kim et al., 2015). It 226
has been shown that external ethylene stimulates leaf senescence (Bleecker et al., 1988; Zacarias & 227
Reid, 1990), while ethylene-insensitive mutants (etr1-1, ers1, ein2-1, ein2-5, ein3-1 and ein3-1 eil1-1 228
in Arabidopsis and Nr in tomato) show a reduced rate of senescence (Bleecker, 1988; Hua et al., 229
1995; Grbic and Bleecker, 1995; Oh et al., 1997; Lanahan et al., 1994, Li et al., 2013; Kim et al., 2014). 230
Both etr1-1 and ein2-1 mutants have increased ethylene production compared to wild-type plants 231
(Guzman & Ecker, 1990; Woeste et al., 1999), yet their insensitivity towards ethylene overturns the 232
additional ethylene, resulting in a delay in leaf senescence. Eventually, ethylene-insensitive mutants 233
age and show senescence, suggesting that ethylene controls both the rate and timing of leaf 234
senescence (Grbic & Bleecker, 1995). Delayed senescence and concomitant decline in chlorophyll 235
content and photosynthesis has also been observed in antisense plants for ACO of tomato (Picton et 236
al., 1993; John et al., 1995; Jensen & Veierskov, 1998) and acs6 mutants of the C4 plant maize 237
(Young et al., 2004), but not for acs mutants of Arabidopsis (Tsuchisaka et al., 2009). Arabidopsis 238
plants continuously exposed to ethylene gas do not display an enhanced rate of senescence (Kieber 239
et al., 1993), but have smaller rosettes, similar to ethylene overproducing and constitutive ethylene 240
sensitive mutants (eto1-1, eto1-13, ctr1-1; Guzaman & Ecker, 1990; Kieber et al., 1993; Christians et 241
al., 2009). Tomato plants constitutively overexpressing ACS also show altered leaf development but 242
no signs of enhanced senescence (Lanahan et al., 1994). In general, we conclude that a temporal 243
exposure to ethylene stimulates leaf senescence in mature leaves, while continuous exposure 244
instead causes altered leaf development. 245
A transient ethylene treatment of mature leaves stimulates senescence by upregulating the 246
expression of senescence-associated genes (SAGs) (Grbic & Bleecker, 1995; Guo et al., 2004; Breeze 247
et al., 2011; Figure 1). Several important SAGs have been shown to play a prominent role in different 248
cellular processes such as programmed cell death, autophagy, chlorophyll catabolism, plastid 249
differentiation, sugar metabolism, and resource allocation (Thomas, 2012; Pujol, 2015). The master 250
transcription factor EIN3 has been identified as an important player in controlling SAGs (Li et al., 251
2013). It can activate the expression of NAP (NAM/ATAF1,2/CUC2) and NAC2 (ORE1/NAC092), two 252
important transcription factors controlling leaf senescence (Woo et al., 2004; Kim et al., 2009; Kim et 253
al., 2014). Furthermore, EIN3 binds to the promotor of the microRNA (miRNA) miR164 and 254
progressively inhibits its expression during leaf development (Li et al., 2013). In turn, miR164 inhibits 255
the expression of the transcription factor NAC2 (Kim et al., 2009; Kim et al., 2014; Li et al., 2013), 256
unraveling a dual feed-forward and feedback regulation of senescence by ethylene through the 257
action of EIN3 (Figure 1). 258
Ethylene exerts a species specific response on photosynthesis 259
Extensive literature review indicates that the negative effects of ethylene on different aspects of 260
photosynthesis for both juvenile non-senescing and mature senescing leaves cannot be generalized 261
across species. Various physiological experiments with different ethylene treatments have revealed 262
a species-specific reduction in photosynthesis in some plants (including important crops), although 263
ethylene has no effect on photosynthesis in other species (Table 1; Pallas & Kays, 1982; Squier et al., 264
1985; Taylor & Gunderson, 1986) In one mustard species (Brassica juncea) ethylene was found to 265
stimulate photosynthesis (Kahn, 2004; Iqbal et al., 2011). Besides the major crops listed in Table 1, 266
ethylene also lowers photosynthesis in other species such as radish (Raphanus sativus), pumpkin 267
(Cucurbita pepo), green foxtail (Setaria viridis), sweet potato (Ipomoea batatas), sunflower 268
(Helianthus annuus), Jerusalem artichoke (Helianthus tuberosus), common cocklebur (Xanthium 269
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7
strumarium), and green ash (Fraxinus pennsylvanica), although ethylene has no significant effect on 270
runner bean (Phaseolus coccineus), common orache (Atriplex patula), touch-me-not (Mimosa 271
pudica) and white clover (Trifolium repens) (Pallas & Kays, 1982; Squier et al., 1985; Taylor & 272
Gunderson, 1986; Woodrow et al., 1989). When investigating these data, it should be noted that 273
differences in treatments, growth conditions, timing of the measurements and/or the 274
developmental stage make it impossible to draw firm conclusions, but the general trend is that 275
ethylene inhibits photosynthesis in non-senescing leaves, or has no effect at all on photosynthesis, 276
with the exception of the Brassica juncea species of mustard. Furthermore, studies on tomato and 277
potato (Solanum tuberosum) have shown that a long term ethylene treatment (several days) and its 278
subsequent recovery phase result in a biphasic response of photosynthesis with alternating periods 279
of improved and attenuated photosynthesis compared to the untreated control (Briede et al., 1992; 280
Dueck et al., 2003). These studies provide preliminary insight into the dynamic temporal regulation 281
of photosynthesis by ethylene in tomato and potato, and stress the importance of the time point of 282
sampling after the treatment. In addition, Woodrow et al. (1989) and Woodrow & Grodzinski (1989) 283
provide evidence that the ethylene-induced reduction of photosynthesis in tomato and common 284
cocklebur is mainly caused by a reduced light perception of leaves as a consequence of the epinastic 285
response induced by ethylene. The orientation of the leaves towards the light source is another 286
important element that influences net photosynthesis. 287
Table 1 and the summary above clearly indicate that our knowledge concerning the influences of 288
ethylene on photosynthesis is mainly derived from C3 species. Whilst several C3 plants are listed, 289
with the exception of maize and green foxtail, C4 plants are unrepresented. C4 photosynthesis in 290
maize seems unaffected by an ethylene treatment (Pallaghy & Raschke, 1972; Taylor & Gunderson, 291
1986; Squier et al., 1985), while natural transposon mutants of ACS6 of maize show reduced 292
ethylene biosynthesis, resulting in higher chlorophyll and Rubisco contents and higher 293
photosynthesis rates (Young et al., 2004). These data suggest that endogenous levels of basal 294
ethylene seem to suppress maximal photosynthetic activity in maize. There are no reports that 295
describe the effect of ethylene on CAM photosynthesis to our knowledge; one manuscript reports 296
ethylene gassing experiments with the C3/CAM intermediate ice plant (Mesembryanthemum 297
crystallinum), but only in the C3 mode (Hurst et al., 2004). As no nocturnal increase in either malic 298
acid or PEPC transcripts could be observed after treatment with 200 ppb ethylene, Hurst et al. 299
(2004) concluded that ethylene was not involved in signaling of the C3-CAM transition. 300
301
Concluding remarks 302
The vital process of photosynthesis supplies plants with energy and carbohydrates and sustains 303
other life on earth by the production of precious oxygen. Over recent decades, tremendous 304
advancements have been made in our understanding of the process of photosynthesis and its 305
adjacent pathways, yet its hormonal regulation by ethylene remains largely unexplored (see also 306
Outstanding Questions Box). This review highlights that ethylene exerts species-specific regulation 307
on plant photosynthesis where it reduces photosynthesis in some species, and has no effect in other 308
species. It must be noted that ethylene exerts a dual action in which it reduces photosynthesis in 309
young photosynthetically active leaves and inhibits photosynthesis in older leaves by the stimulation 310
of leaf senescence. We have updated the recent findings on how ethylene interferes in different key 311
processes such as chlorophyll biosynthesis, light reactions, stomatal conductance, carboxylation 312
events, carbohydrate partitioning and leaf senescence. The precise mechanisms of how ethylene 313
controls these processes remain only superficially investigated and more research efforts are needed 314
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8
to create a profound understanding how ethylene controls one of the most vital processes in plants. 315
In the long term, this knowledge should be translated into biotechnological applications that benefit 316
agriculture. 317
318
Acknowledgements 319
J.C. and B.V.d.P. both thank KU Leuven Internal Funds for financial support and the reviewers for 320
their constructive comments. 321
322
Tables 323
Table 1. Overview of studies that investigate the role of ethylene on net photosynthesis and/or stomatal 324
conductance in different crop species. 325
Species Ethylene treatment
Conditions (PAR and CO2) Sample Plant age
Net photosyn-thesis (PN)
Stomatal conductance (g) Reference
Arachis hypogaea
(C3)
1 ppm ethylene
340 µmol.m-2
.s 350 ppm CO2
1st fully
expanded leaf 1-2 months Decrease Decrease Pallas & Kays,
1982 1-21 ppm ethylene
325 µmol.m-2
.s 318 ppm CO2
Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985
Brassica juncea (C3)
1.5 mM ethephon
1050 µmol.m-2
.s 360 ppm CO2
New fully expanded leaf
45 days Increase Increase Khan, 2004
400 ppm ethephon
1008 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
80 days Decrease Decrease Kahn et al., 2008
200 ppm ethephon
680 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
50 days Increase Increase Iqbal et al., 2011
Glycine max (C3)
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks Decrease Decrease Taylor & Gunderson, 1986
10 ppm ethylene
460 µmol.m-2
.s CO2 n.s.
1st leaf pair 2-3 weeks Decrease Decrease Gunderson &
Taylor, 1991 3.5 ppm
ethylene 338 µmol.m
-2.s
350 ppm CO2 1
st leaf pair 2-32 weeks Decrease Decrease Taylor &
Gunderson, 1988 1-21 ppm
ethylene 325 µmol.m
-2.s
318 ppm CO2 Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985
Gossypium hirsutum (C3)
0.28 kg.ha-
1 ethephon Open field New fully
expanded leaf Early season
Decrease Decrease Pettigrew et al., 1992
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks Decrease Decrease Taylor & Gunderson, 1986
Phaseolus vulgaris (C3)
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks Decrease Decrease Taylor & Gunderson, 1986
1 ppm ethylene
340 µmol.m-2
.s 350 ppm CO2
1st fully
expanded leaf 1-2 months No effect - Pallas & Kays,
1982 1500 ppm
ethephon n.s. Greenhouse conditions
5 leaves 3 months - Decrease Vitagliano & Hoad, 1978
Pisum sativum (C3)
1-10.000 ppm ethylene
1500 µmol.m-2
.s 288 ppm CO2
5th
leaf 20-25 days No effect No effect Pallaghy & Raschke, 1972
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks No effect No effect Taylor & Gunderson, 1986
1 ppm ethylene
340 µmol.m-2
.s 350 ppm CO2
1st fully
expanded leaf 1-2 months No effect - Pallas & Kays,
1982 Nicotiana tabacum
(C3)
1-21 ppm ethylene
325 µmol.m-2
.s 318 ppm CO2
Whole plant 5-7 weeks Decrease Decrease Squier et al., 1985
Solanum lycopersicum
(C3)
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks Decrease No effect Taylor & Gunderson, 1986
300 g.m-3
ethephon
800 µmol.m-2
.s 335 ppm CO2
Whole plant 11-12 leaves
Decrease - Woodrow & Grodzinski, 1989
2 mM ethephon
700 µmol.m-2
.s 300 ppm
New fully expanded leaf
11-12 leaves
No effect No effect Woodrow et al., 1988
Solanum tuberosum (C3)
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks No effect Decrease Taylor & Gunderson, 1986
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9
1 ppm ethylene
340 µmol.m-2
.s 350 ppm CO2
1st fully
expanded leaf 1-2 months No effect - Pallas & Kays,
1982 1-10 ppm
ethylene 1000 µmol.m
-2.s
340 ppm CO2 New fully expanded leaf
3-4 weeks Decrease Decrease Govindarajan & Poovaiah, 1982
5 ppm ethephon
1200 µmol.m-2
.s CO2 n.s.
1st fully
expanded leaf 30 cm tall plants
Biphasic Increase Briede et al., 1992
450 ppb ethylene
Open field conditions
Whole plant 3.5 weeks Decrease Decrease Dueck et al., 2003
Triticum aestivum
(C3)
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks No effect Decrease Taylor & Gunderson, 1986
50 mM ethephon
1200 µmol.m-2
.s Open field CO2
Flag leaf Flowering plants
No effect Increase Yang et al., 2014
Zea mays (C4)
1-10.000 ppm ethylene
1500 µmol.m-2
.s 288 ppm CO2
5th
leaf 20-25 days No effect No effect Pallaghy & Raschke, 1972
5.1 ppm ethylene
510 µmol.m-2
.s CO2 n.s.
New fully expanded leaf
3-8 weeks No effect No effect Taylor & Gunderson, 1986
1-21 ppm ethylene
325 µmol.m-2
.s 318 ppm CO2
Whole plant 5-7 weeks - No effect Squier et al., 1985
n.s.: not specified; 326
327
Figure legends 328
Figure 1. Overview of the regulatory effects of ethylene on plant photosynthesis and its features for 329 juvenile/non-senescing and mature/senescing leaves. Because the regulation of photosynthesis is species-330 specific, this general scheme does not apply to every species, but merely reflects the general mode of action 331 for the inhibitory effect of ethylene on photosynthesis as found in Arabidopsis. ABA, abscisic acid; CTR1, 332 CONSTITUTIVE TRIPLE RESPONSE 1; EIN2, ETHYLENE INSENSITIVE 2; EIN3, ETHYLENE INSENSITIVE 3; EIL, EIN3-333 LIKE; ERF, ethylene response factors; ETR, ethylene receptor; H2O2, hydrogen peroxide; PAG, 334 photosynthetically active genes; ROS, reactive oxygen species; SAG, senescence-associated gene. 335
Figure 2. Overview of the three modes of photosynthesis (C3, C4 and CAM) in plants, indicating the importance 336 of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC) 337 as main enzymes involved in carbon fixation. 338
Figure 3. Overview of the plant ethylene signal transduction pathway. Ethylene binds the ethylene receptors 339
(ETR) at the endoplasmic reticulum (ER) resulting in auto-phosphorylation of the receptor and inactivation of 340
the downstream kinase CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1). In the absence of ethylene CTR1 341
phosphorylates the ER localized ETHYLENE INSENSITIVE 2 (EIN2) directing it for proteasomal degradation by 342
the ETPs. When ethylene is present, the EIN2 C-terminal part (EIN2-C) is not phosphorylated and gets cleaved 343
and migrates to the nucleus, where it activates the master transcription factor ETHYLENE INSENSITIVE 3 (EIN3) 344
and EIN3-likes (EILs). In the absence of ethylene, EIN3 and EILs are targeted for proteasomal degradation by 345
the ETHYLENE BINDING FACTOR (EBF). EIN3 and EILs on their turn activate ethylene response factors (ERFs) or 346
ethylene responsive genes. The EIN2-C can also interact with the mRNA of selected transcripts, including the 347
5’UTR of the EBF mRNA, to inhibit translation. 348
349
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Juvenile/non-senescing leaves Mature/senescing leaves
ETR
CTR1
Ethylene
EIN2
EIN3/EILs
ERFs
PAG
PS I & II efficiency
Chlorophyll contentETR
CTR1
Ethylene
EIN2
EIN3/EILs
ERFs
SAG
Chlorophyll catabolism
Stress
Photosynthesis Photosynthesis
ABA
Flavonols
Stomatal closureROS (H2O2)
Chlorophyll biosynthesis
miR164
Glucose/sugars
Sugar partitioning
Rubisco
Figure 1. General overview of the regulatory effects of ethylene on plant photosynthesis and
sub-elements that are likely to co-regulate photosynthesis for both juvenile/non-senescing and
mature/senescing leaves. Because the regulation of photosynthesis is species-specific, this gen-
eral scheme does not apply to every species (e.g. ethylene stimulates photosynthesis in mus-
tard), but merely reflects the general mode of action for the inhibitory effect of ethylene on
photosynthesis. ABA, Abscisic acid; CTR1, CONSTITUTIVE TRIPPLE RESPONSE 1; EIN2, ETHYLENE
INSENSITIVE 2; EIN3, ETHYLENE INSENSITIVE 3; EILs, EIN3-likes; ERF, ethylene response factors;
ETR, ethylene receptor; PAG, photosynthetically active genes; ROS, reactive oxygen species; SAG,
senescence associated genes.
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C3 plants C4 plants CAM plants
Calvin
cycle
Glyceraldehyde
3-phosphate
CO2
Mesophyll
cell
Calvin
cycle
CO2
Bundle
sheath
cell
Malic acid (C4)Mesophyll
cell
CO2
CO2
Calvin
cycle
CO2
Malic acid (C4)
Mesophyll
cell
CO2
Night
Day
Rubisco
PEPC PEPC
Rubisco Rubisco
Glyceraldehyde
3-phosphate
Glyceraldehyde
3-phosphate
Sucrose Sucrose Sucrose
Figure 2. Simplified overview of the three modes of photo-
synthesis (C3, C4 and CAM) in plants, indicating the impor-
tance of ribulose-1,5-bisphosphate carboxylase/oxygenase
(Rubisco) and phosphoenolpyruvate carboxylase (PEPC) as
main enzymes involved in carbon fixation.
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P P
P
P P
P
CH
HC
H
H
ETREIN2
CTR1
ETP
EIN3EIN3
EBF
EIN2-C
ERFs
ER
Nucleus
ER lumen
Cytosol
NO ETHYLENE ETHYLENE
EBF
Ethylene responsive genes
EBF mRNA
EIN2-C
EIN2
CTR1
ETRC
H
HC
H
H
CH
HC
H
H
CH
HC
H
H
Figure 3. General overview of the plant ethylene signaling transduction pathway. Ethylene binds with the
ethylene receptors (ETR) at the endoplasmic reticulum (ER) resulting in auto-phosphorylation of the receptor
and inactivation of the downstream kinase CONSTITUTIVE TRIPPLE RESPONSE 1 (CTR1). In the absence of
ethylene CTR1 phosphorylates the ER localized ETHYLENE INSENSITIVE 2 (EIN2) directing it for proteasomal
degradation by the ETPs. When ethylene is present, the EIN2 C-terminal part (EIN2-C) is not phosphorylated
and gets cleaved and migrates to the nucleus, where it activates the master transcription factor ETHYLENE
INSENSITIVE 3 (EIN3) and EIN3-likes (EILs). In the absence of ethylene, EIN3 and EILs are readily targeted for
proteasomal degradation by the ETHYLENE BINDING FACTOR (EBF). EIN3 and EILs on their turn activate
ethylene response factors (ERFs) or ethylene responsive genes. The EIN2-C can also interact with the mRNA of
selected transcripts, including the 5’UTR of the EBF mRNA, to inhibit translation.
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BOX 1. Photosynthetic Pathways in Plants
Photosynthesis involves the light-mediated conversion of inorganic substrates (i.e. carbon dioxide and water) into organic compounds and occurs via three pathways in terrestrial plants (Fig. 2). C3 is the ancient and most common pathway, found in about 93% of plant species. C3 photosynthesis relies on direct CO2 fixation during the light period in the chloroplasts, mediated by the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). C4 and crassulacean acid metabolism (CAM) can be regarded as evolutionary adaptive mechanisms of photosynthesis that enhance the CO2 concentration at the Rubisco carboxylation site, thus helping plants adapt to the pronounced reduction in CO2 and rise in O2 levels that started about 350 million years ago (Baars, 2017). Both modes of photosynthesis deploy the same machinery present in C3 plants, but differ in the initial mode of carboxylation (West-Eberhard et al., 2011). Carbon uptake in C4 plants (about 1% of plant species) uses diurnal activity of phosphoenolpyruvate carboxylase (PEPC) in the leaf mesophyll cells followed by decarboxylation of the synthesized malic acid in the chloroplasts of bundle sheath cells where Rubisco activity is enhanced by achieving high internal CO2 concentrations (Sage et al., 2012). CAM plants (about 6% of plant species) employ a temporal separation between carboxylation events, allowing initial nocturnal CO2 sequestration by PEPC followed by Rubisco-mediated carboxylation during daytime behind closed stomata, thereby conserving considerable amounts of water (Borland et al., 2011).
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BOX 2. Ethylene Biosynthesis and Signaling in
Plants
Ethylene is a gaseous hormone that can easily migrate from cell to cell, gradually diffusing throughout the tissue and regulating ethylene-responsive processes (Fig. 3). Most of the ethylene signaling pathway was unraveled by screening for ethylene-related mutants in dark-grown seedlings (triple response) of Arabidopsis (Merchante and Stepanova, 2017). In the light, these mutants have different phenotypes, such as altered photosynthesis. Screening for light-specific ethylene mutants can provide new insights into how ethylene regulates photosynthesis. Ethylene is produced from the precursor 1-aminocyclopropane-1-carboxylic acid (ACC; Adams and Yang, 1979) by the dioxygenase ACC-oxidase (ACO; Ververidis and John, 1991). ACC is synthesized from S-adenosyl-L-methionine by ACC-synthase (ACS; Adams and Yang, 1977; Boller et al., 1979). The synthesized ethylene can bind to the ethylene receptor (Bleecker et al., 1988), a two-component receptor kinase (Chang et al., 1993) located at the endoplasmic reticulum (ER; Chen et al., 2002) forming active hetero- and homodimers (Schaller et al., 1995; Bakshi et al., 2015). Ethylene binding to the active site promotes autophosphorylation of the receptor (Moussatche and Klee, 2004; Bisson and Groth, 2010) and inactivation of the downstream kinase CONSTITUTIVE TRIPLE RESPONSE1 (CTR1; Kieber et al., 1993). Active CTR1 kinase phosphorylates
ETHYLENE INSENSITIVE2 (EIN2; Ju et al., 2012), an ER-bound N-ramp protein (Alonso et al., 1999), which is subsequently targeted for proteasomal degradation by two F-box proteins, EIN2 TARGETING PROTEIN1 (ETP1) and ETP2 (Qiao et al., 2009). When ethylene is bound to its receptor, EIN2 is not phosphorylated and gets cleaved by an unknown protease (Qiao et al., 2012). After cleavage, the EIN2 C-terminal fragment migrates to the nucleus (Ju et al., 2012; Qiao et al., 2012; Wen et al., 2012). There, the C-terminal end activates the master transcription factor EIN3 (Roman et al., 1995; Chao et al., 1998) and its homologs EIN3-LIKE1-3 (EIL1-3) (Chao et al., 1998). In the absence of ethylene, EIN3 and EILs are rapidly turned over by proteasomal degradation through the action of two F-box proteins ETHYLENE BINDING FACTOR1 (EBF1) and EBF2 (Guo and Ecker, 2003; Potuschak et al., 2003; Gagne et al., 2004; An et al., 2010). Recent work also demonstrated that the EIN2 C-terminal end inhibits translation of the EBFs through interaction with their 5′UTR mRNA region, which blocks ribosomal activity (Merchante et al., 2015; Li et al., 2015). Activated EIN3 and EILs bind to an ethylene binding sequence in ethylene-responsive genes, of which the ETHYLENE RESPONSIVE FACTORS (Solano et al., 1998) encode downstream secondary transcription factors that induce ethylene-responsive gene expression (Nemhouser et al., 2006; Chang et al., 2013).
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ADVANCES
• Integrating available surveys of different plant species reveals a species-specific regulation of photosynthesis by ethylene. Ethylene inhibits photosynthesis in some plants, but not in others, and was found to stimulate photosynthesis in only mustard (Brassica juncea).
• Ethylene interacts with photosynthesis at different mechanistic levels by influencing transcription, translation, and key enzyme activities implicated in chlorophyll synthesis, stomatal conductance, light capture, electron transport, carbon fixation, and carbohydrate partitioning.
• Ethylene cross talks with sugar metabolism to fine tune feedback mechanisms of photosynthesis.
• The ethylene master transcription factors EIN3/EIL control SAG genes and senescence-associated microRNAs in senescing leaves as well as PAG genes in juvenile leaves.
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OUTSTANDING QUESTIONS
• Why is the action of ethylene on photosynthesis species-specific? Other ethylene-regulated processes are also species-specific, such as hyponasty, epinasty, aerenchyma formation, climacteric fruit ripening, etc., but we lack a comprehensive physiological explanation.
• What are the downstream ethylene-responsive transcription factors that control photosynthesis-related gene expression?
• What is the effect of ethylene on the initial carboxylation mediated by CA and PEPC in C4 and CAM plants?
• How does ethylene influence carbohydrate partitioning in photosynthesizing leaves?
• Ethylene triggers leaf senescence and thus reduces photosynthesis in an age-dependent manner. What are developmental cues that control this age-dependent regulatory role of ethylene on leaf senescence?
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