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Update Review 1

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Short title: 3

Flower Central Metabolism 4

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Corresponding author: 6

Monica Borghi 7

ORCID ID: 0000-0003-1359-7611 8

Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany. 9

E-mail: MBorghi@mpimp-golm.mpg.de 10

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Title: 12

Floral Metabolism of Sugars and Amino Acids: Implications for Pollinators’ Preferences and 13

Seed and Fruit Set 14

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Authors’ names: 16

Monica Borghi 17

Alisdair R. Fernie 18

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Authors’ affiliation: 20

Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany. 21

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Funding: 23

This work was supported by the Marie Skłodowska-Curie Actions Individual Fellowship program 24

(grant no. 656918 to M.B.). 25

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Plant Physiology Preview. Published on October 6, 2017, as DOI:10.1104/pp.17.01164

Copyright 2017 by the American Society of Plant Biologists

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Corresponding author e-mail: 27

MBorghi@mpimp-golm.mpg.de 28

Summary: New discoveries open up future directions in the study of the primary 29

metabolism of flowers. 30

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Abstract 34

Primary metabolism in flowers sustains a plenitude of physiological and ecological 35

functions related to floral development and plant reproduction. Carbohydrates and amino 36

acids provide energy and precursors for the reactions of floral secondary metabolism, 37

such as the molecules for color and scent, and constitute an important resource of food 38

for the pollinators. Recent discoveries have advanced our understanding of the cycles of 39

carbohydrate hydrolysis and re-synthesis that regulate pollen development, pollen tube 40

growth, and pollination, as well as the composition of nectar. Pathways of de novo amino 41

acid biosynthesis have been described in flowers, and the proteins that regulate pollen 42

tube guidance and ultimately control fertilization are being progressively characterized. 43

Finally, a novel field of research is emerging that investigates the chemical modification 44

of sugars and amino acids by colonizing microorganisms and how these affect the 45

pollinators' preferences for the flowers. In this Update article, we provide an overview of 46

the new discoveries and future directions concerning the study of the primary metabolism 47

of flowers. 48

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4

Title: 53

Floral Metabolism of Sugars and Amino Acids: Implications for Pollinators’ Preferences and 54

Seed and Fruit Set 55

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Introduction 58

The chemistry of flowers is unique as it sustains very diverse physiological functions such as 59

flower development, the transition from flower to fruit and the initial phases of seed set (O'Neill, 60

1997; Pélabon et al., 2015). In addition, floral metabolites fulfill relevant ecological roles such as 61

acting as signaling molecules in the chemical communication with animal pollinators (Borghi et 62

al., 2017), providing protection against pests and colonizing microorganisms (Kessler and 63

Baldwin, 2007; Nepi, 2014). Stunning displays of the metabolic resources of flowers are, for 64

example, their colors and fragrance, which occur following the accumulation and emission of 65

tinted and scented secondary metabolites, respectively (Grotewold, 2006; Tanaka et al., 2008; 66

Khan and Giridhar, 2015). Perhaps less sensational, but as equally as important, are the reactions 67

of primary metabolism. Indeed these sustain the physiology of flowers, provide the chemical 68

precursors, and meet the energy demand of floral secondary metabolism (Muhlemann et al., 69

2014). Moreover, sugars and amino acids also serve as a nutritional reward for the pollinators that 70

feed on nectar and pollen (Pacini et al., 2006; Heil, 2011; Roy et al., 2017). Therefore knowing 71

how primary metabolites are imported or de novo synthesized in flowers, and how they are 72

secreted and catabolized is at the heart of floral biology being relevant to understand the 73

physiology of plant reproduction and the role that flowers play in the ecosystem. In this article, 74

we aim to provide an overview of floral central metabolism. How primary metabolism sustains 75

flower development, and fruit and seed set will also be addressed. Finally, given the considerable 76

proportion of primary metabolites that are channeled into nectar, we will discuss the chemical 77

composition of nectar, the modifications that arise from fermentation processes by colonizing 78

5

yeasts and bacteria, and the impact that these modifications have on pollinators’ preferences for 79

flowers. 80

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The path of sugars toward the flower 83

As photosynthesis in flowers is confined to sepals and young petals, floral tissues rely heavily on 84

the source-to-sink flow for the supply of carbon resources (Müller et al., 2010). Experiments 85

performed in the early ‘70s with cut carnation flowers revealed that sucrose is the sugar 86

preferentially transported alongside the flower-peduncle across the phloem (Ho and Nichols, 87

1975). However, it was not until much later that the transporter proteins (and the genes which 88

encode them), regulating phloem loading and unloading were discovered and described in detail. 89

It is now known that in source tissues (mature leaves) sucrose is loaded into the phloem by the 90

coordinated activity of SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER 91

(SWEET) and SUCROSE UPTAKE CARRIER (SUC) which are alternatively called SUCROSE 92

UPTAKE TRANSPORTER (SUT) proteins, therefore we will be referring to this family as 93

SUC/SUT. SWEETs are efflux proteins of the plasma membrane, tonoplast, and Golgi that 94

transport sucrose and hexoses (Eom et al., 2015; Feng and Frommer, 2015), and SUC/SUTs are 95

plasma membrane localized proton-sucrose symporters of the Major Facilitator Superfamily 96

(MFS) of cotransporters (Lalonde et al., 2004). In leaves of Arabidopsis thaliana SWEET11 and 97

SWEET12 are the proteins that export sucrose from the parenchyma cells and provide it to SUT1 98

for phloem loading (Chen et al., 2012). 99

Flowers are strong sinks that draw sucrose and nutrients toward them. The gradient that maintains 100

this upward flow is generated in the flower by a series of phloem unloading events and post-101

phloem distribution of photoassimilates to developing organs and tissues. Symplasmic and 102

apoplasmic retrieval of sucrose have both been documented in flowers and they reflect the pattern 103

of floral development and the physiological needs of the newly formed tissues (Muller et al., 104

6

2010). Indeed, early studies conducted with symplasmic tracers revealed that the trafficking 105

toward the apical meristem decreases after floral induction (Gisel et al., 2002), while the 106

expression and activity of sugar transporters progressively increase while pollen mature and after 107

fertilization has occurred (Gahrtz et al., 1996). 108

Symplasmic phloem unloading and post-phloem transport requires functional plasmodesmata, 109

and it primarily occurs in petals, along the filament that provides nutrients to the connective tissue 110

of the anthers and across the funiculus (Imlau et al., 1999). A wave of symplasmic post-phloem 111

transport has also been observed in young flowers during ovule development (bud stages) and in 112

mature flowers shortly after anthesis, and it seemingly mirrors the de novo formation of new 113

plasmodesmata and morphological adjustments of pre-existing connections (Werner et al., 2011). 114

Apoplasmic phloem unloading and post-phloem transport requires energy and the intervention of 115

protein carriers to transport sucrose across the plasma membrane. In flowers, this occurs in 116

symplasmically isolated tissues such as pollen grains and tubes, as well as developing embryos. 117

The longstanding model of apoplasmic phloem transport describes this flow as a two-step process 118

in which sucrose is initially unloaded from the sieve elements into the apoplasm and subsequently 119

transported inside the sink cells. Proteins of the SWEET and SUC/SUT families that facilitate the 120

upload of sucrose in specific floral tissues have been characterized (see below), while carriers 121

acting in the floral receptacle to export sucrose from the cells of terminal phloem have not yet 122

been identified. In this regard, SWEET efflux transporters, whose expression in floral tissues is 123

well documented, are putative candidates (Lin et al., 2014; Eom et al., 2015) (Fig. 1A). 124

Carbon is unloaded in target cells in the form of sucrose or alternatively following its hydrolysis, 125

as fructose and glucose. In the apoplasmic space, the hydrolysis of sucrose is catalyzed by 126

invertases ionically bound to the wall of the surrounding cells and for this reason named cell wall 127

invertases (cwINV) (Ruan et al., 2010). These are enzymes of the -fructofuranosidase family 128

which catalyze the hydrolysis of terminal units of fructose from molecules of di- and poly-129

saccharides and contribute to creating the concentration gradient that allows sucrose to be 130

7

unloaded from the phloem and effectively partitioned among target floral tissues. In addition to 131

cwINVs, flowers also express vacuolar (VIN) and cytoplasmic invertases (CIN), the latter being 132

sensu stricto sucrose invertases (Ruan et al., 2010). Finally, plasma membrane SUGAR 133

TRANSPORTER PROTEINS (STPs) are also expressed in flowers and mediate the uptake of the 134

hexoses released in the apoplasmic space (Büttner, 2010). 135

A high rate of sugar import is required to meet the respiratory demand of floral tissues, and 136

indeed high rates of respiration have commonly been documented in floral organs (Dickinson, 137

1965; Hew and Yip, 1991; Karapanos et al., 2010). Rates of respiration are exceptionally high in 138

flowers of plants that carry out thermogenesis, such as the Araceae family including skunk 139

cabbage and voodoo lily, which produce a raceme type of unbranched inflorescence known as 140

spadix (Plaxton and Podestá, 2006). On anthesis, the plenitude of mitochondria of the spadix 141

contributes to enormous respiration rates via the alternative oxidase pathway (Seymour, 1999), 142

which releases free energy as heat being equivalent to a 10-25°C increase in tissue temperature. 143

This process serves two functions. Firstly, it supports the extreme growth rates of the spadix 144

(Dancer and ap Rees, 1989). Secondly, it is thought that the temperature aids in the production 145

and volatilization of floral scents (Seymour, 1999), a process that is also aided by the high content 146

of organic acids of the spadix. This striking specific example aside, little is known concerning the 147

relative activities of organic acid metabolism in these tissues (Borghi et al., 2017), hence the 148

sections below focus on sugars and amino acids for which our spatial understanding is far more 149

developed. 150

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152

Carbohydrate Partitioning and Metabolism in Floral Organs 153

The paragraphs that follow provide the description of primary metabolism organized by floral 154

organs. Sepals that are similar to leaves in their anatomy and metabolism are not discussed, and 155

8

we refer to reviews on leaf metabolism instead (Plaxton and Podestá, 2006; Smith and Stitt, 156

2007). 157

158

All floral organs - with the exception of sepals – depend upon sugar import in a measure that 159

correlates with their growth and stage of development and are mainly sustained by post-phloem 160

sucrose delivery and only to a minor extent by carbohydrates produced via floral carbon fixation 161

(Aschan and Pfanz, 2003). In regard to metabolism, petals are mixotrophic: young green petals 162

are able to perform photosynthesis but they progressively lose the ability to fix carbon as they 163

mature and ultimately become fully heterotrophic (Thomas et al., 2003). For example, the corolla 164

of young Nicotiana tabacum flowers contains chlorophylls and an active Rubisco enzyme which 165

both contribute to carbon acquisition. However, at the onset of anthesis, the rate of photosynthesis 166

progressively decreases while pigments gradually accumulate from the distal part of the perianth 167

inwards (Müller et al., 2010). Indeed, a biochemical reprogramming occurring at (or around) 168

anthesis has been documented in numerous plant species. For example, in petals of Antirrhinum 169

majus (snapdragon) chlorophyll content decreases at the anthesis (Muhlemann et al., 2012), and 170

similarly, in A. thaliana, the dismantling of the photosynthetic apparatus, which follows the 171

conversion of chloroplasts to chromoplasts starts soon after the flowers open (Wagstaff et al., 172

2009). This shift from autotrophic to heterotrophic metabolism is transcriptionally regulated and 173

marks the moment when flower secondary metabolism becomes predominant (Muhlemann et al., 174

2012; Tsanakas et al., 2014). As glycolysis and the pentose phosphate pathway are 175

transcriptionally down-regulated and floral secondary metabolic pathways up-regulated, the 176

concentration of metabolic intermediates of the tricarboxylic acid (TCA) cycle such as fumarate 177

and malate also declines, while the content of volatile organic compound (VOC) precursors, such 178

as for example the aromatic amino acids phenylalanine and tyrosine progressively increases 179

(Muhlemann et al., 2012). Indeed, the physiological function of petals is that to attract animal 180

pollinators to flowers, for which pigments and scented molecules are synthesized. Therefore, the 181

9

transcriptional co-regulation of primary and secondary metabolism ensures that the energy 182

requirements and precursors for the biosynthesis of secondary metabolites are in place when this 183

switch occurs. 184

Petals also store carbohydrates that serve an important function during flower opening. For this, 185

reserve polysaccharides (starch and/or fructans) are gradually accumulated during petal 186

development but rapidly degraded at the onset of anthesis to generate the osmotic potential that 187

leads to cellular water influx and finally to flower opening (Bieleski, 1993; Collier, 1997; van 188

Doorn and van Meeteren, 2003; van Doorn and Kamdee, 2014). As plasmodesmata are functional 189

in young petals, symplasmic post-phloem sucrose is arguably the prime supplier of these reserves, 190

although sucrose carriers may also contribute. In this regard, it is worth to mention that the 191

proton-monosaccharide symporter SUT13 that transports glucose, fructose, and other D-hexoses is 192

highly expressed in the vasculature of young emerging petals (Nørholm et al., 2006) and may 193

therefore also participate in hexose unloading in target cells. 194

195

Androecium and gynoecium are fully heterotrophic, that is their metabolism and growth are 196

entirely supported by the carbon resources synthesized in source tissues. 197

In the androecium (stamen) photoassimilates are delivered to the anthers through the filament, a 198

duct of vascular tissue that symplasmically connects the anthers to the flower (Mascarenhas, 199

1989). Carbon unloaded from the filament is stored as granules of starch and soluble sugars 200

(primarily sucrose) in the tapetum, a layer of nutritive cells that develops between the anther wall 201

and the sporogenous tissue (Goldberg et al., 1993). In certain plant species, such as tomato, 202

sucrose is partially hydrolyzed to glucose and fructose while being transported along the filament, 203

so that hexoses are readily available as they reach the anther wall (Pressman et al., 2012) (Fig. 204

1B). Otherwise, sucrose synthase (SUS) in the tapetum cleaves sucrose before uptake, while in 205

the cytoplasm of the same cells sucrose phosphate synthase (SPS) and sucrose phosphate 206

phosphatase (SPP) re-synthesize it once again (Fig. 1C) (Pacini et al., 1985; Hedhly et al., 2016). 207

10

Due to the presence of this “futile cycle” of sucrose breakdown and re-synthesis (Geigenberger 208

and Stitt, 1991; Nguyen-Quoc and Foyer, 2001), it has been proposed that the tapetum has a 209

buffering function that regulates sugars availability in the whole anther (Castro and Clément, 210

2007). As anthers develop, sugar resources are mobilized and exported to the locular fluid that 211

surrounds and nourishes the pollen grains while the tapetum slowly degenerates (Pacini et al., 212

1985). Pollen grains are symplasmically isolated from the surrounding tissues and rely upon 213

plasma membrane transporters for sugars intake. During the course of evolution, this complete 214

dependence on apoplasmic transport has given rise to a myriad of pollen specific sugar carriers 215

that mediate pollen sugars uptake during development, germination, and pollen tube growth 216

(Table 1 provides an overview of sugar transporters characterized in A. thaliana and their site(s) 217

of floral expression). Immature pollen grains utilize sugars for cell wall synthesis, as well as to 218

build up the carbon reserves that will be utilized during germination (Hafidh et al., 2016). In the 219

initial phase of development, cwINVs bound to the wall of pollen grains and SUS enzymes 220

hydrolyze sucrose from the locular fluid (Goetz et al., 2001; Persia et al., 2008; Hirsche et al., 221

2009; Le Roy et al., 2013; Carrizo García et al., 2015), while STP transporters facilitate the 222

uptake of the units of glucose that are released in these reactions (Truernit et al., 1996). Fructose, 223

which is also released from the breakdown of sucrose, is primarily internalized by POLYOL-224

MONOSACCHARIDE TRANSPORTER (PMT) 1 (Klepek et al., 2009), and to a minor extent 225

by STPs (Hedhly et al., 2016). However, the fructose to glucose ratio in the apoplasmic space that 226

surrounds the wall of pollen grains is above two implying a preferential uptake of glucose 227

(Pressman et al., 2012). Non-hydrolyzed sucrose is most probably internalized by SWEET8 (Fig. 228

1D) (Chen et al., 2012). During pollen maturation the GLUCOSE PHOSPHATE 229

TRANSPORTER 1 (GPT1) transports glucose-6-phosphate across the outer membrane of 230

amyloplasts for starch biosynthesis (Pacini et al., 1985; Niewiadomski et al., 2005; Castro and 231

Clément, 2007). Alternatively, carbohydrates are utilized for the synthesis of pollen cell wall. At 232

the beginning of their development, pollen grains of all plant species accumulate starch in 233

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amyloplasts, which it is later partially or completely converted to sucrose, other sugar polymers 234

and sometimes lipids that are either stored in small vacuoles or freely deposited in the cytoplasm 235

(Fig. 1D). VACUOLAR GLUCOSE TRANSPORTER 1 (VGT1) may be involved in this process as 236

it moves glucose across the tonoplast and is highly expressed in the pollen grains (Aluri and 237

Büttner, 2007). The presence of starch in mature pollen negatively correlates with pollen 238

longevity and is used as an indicator of pollination type (Franchi et al., 2011). In fact, starchy 239

short-lived pollen is partially hydrated and readily collected for dispersal by animal pollinators. 240

This type of pollen is referred to as recalcitrant pollen since it does not require dormancy and 241

quickly germinates when deposited on a permissive stigma (Franchi et al., 2011). Conversely, 242

pollen grains rich in sucrose are dry and long-lived and are produced by plant species well 243

adapted to arid climates (Hoekstra et al., 1989; Franchi et al., 1996; Nepi et al., 2001). Once 244

pollen is mature, the anther wall breaks and pollen grains are released. The rupture of the anther 245

wall also depends upon sugar metabolism and it is attained by raising the osmotic potential of the 246

cells at the junction between the anthers and filament, a process presumably promoted by the 247

activities of VIN (Wang and Ruan, 2016) and SUC1 (Singh and Knox, 1984; Stadler et al., 1999). 248

249

Pollination is characterized by an intense sugar turnover. In fact, once the pollen grain reaches the 250

stigma and rehydrates, sugar resources are mobilized, the pollen tube emerges and starts to 251

elongate inside the transmitting tissue of the style (Rounds et al., 2011). As ovules are usually 252

born at the base of the carpel, frequently one to few centimeters from the stigma, rehydrated 253

pollen grains rapidly grow a long tube to deliver sperms for the process of fertilization. Tube 254

elongation is supported by a rapid and intense deposition of plasma membrane and new cell wall 255

material at the tip of the tube, for which sugars provide building blocks (Konar and Linskens, 256

1966) and energy (Ylstra et al., 1998). Pollen germinates in a sugar-rich environment (Labarca et 257

al., 1970) that boosts glycolysis (Carrizo García et al., 2015) to produce abundant pyruvate to be 258

flown through the TCA cycle for ATP production. It has been discovered that aerobic 259

12

fermentation also supports pollen tube growth. For this, a series of cytosolic reactions collectively 260

referred to as the pyruvate dehydrogenase (PDH) bypass convert pyruvate to acetyl-CoA, which 261

is then transported to mitochondria (TCA cycle) and glyoxysomes (glyoxylate pathway), or 262

utilized for the synthesis of lipids (Gass et al., 2005; Rounds et al., 2011). The PDH bypass 263

confers the evolutionary advantage of fast-growth to pollen grains that germinate onto permissive 264

stigmas so that wild-type pollen out-competes PDH bypass defective mutants. This extensive 265

uptake of sugars in elongating pollen tubes is mediated by SUC/SUT transporters, and the activity 266

of STPs, PMTs, and cwINVs (Mascarenhas, 1970; Singh and Knox, 1984; Truernit et al., 1996; 267

Ylstra et al., 1998; Stadler et al., 1999; Schneidereit et al., 2003; Scholz-Starke et al., 2003; 268

Schneidereit et al., 2005; Klepek et al., 2009; Büttner, 2010). Recently, it was found that the 269

combined activities of cwINVs on the cell wall of pollen tubes and VINs in the cells of the 270

transmitting tissue of the style also promote proper tube elongation (Fig. 1E). Indeed, VINs in the 271

female tissues show a wave of activation that chases up closely the growth of the pollen tube, so 272

that sugar resources are rapidly made available as the tip of the tube moves forward along the 273

style (Goetz et al., 2017). The discovery of this mutual interaction adds one more tile to the 274

mosaic of molecular mechanisms that regulate a long time known phenomenon that is the 275

appearance of random elongation trajectories and slow growth rates observed in pollen grains 276

germinated in vitro. 277

278

The gynoecium (pistil) is composed of one or more carpels, each consisting of a stigma, style, 279

and ovary. The metabolic activity of each part of the pistil specifies its physiological function, 280

correlates with flower development and is subject to transcriptional regulation. Indeed, analysis of 281

transcripts levels in pollinated and unpollinated pistils of A. thaliana revealed that pollination, 282

precisely the transfer of pollen grains to a compatible stigma, triggers the metabolic switch that 283

assists flower fertilization (Boavida et al., 2011). While flowers develop, the pistil 284

symplasmically receives sucrose from source tissues and stores it as transitory starch at the base 285

13

of the carpel, and alongside the style up to the base of the stigma (Hedhly et al., 2016). It is 286

accepted that glucose-6-phosphate/phosphate antiporter is responsible for carrying glucose across 287

the outer membrane of plastids to support the progressive enlargement of starch granules 288

(Dresselhaus and Franklin-Tong, 2013). 289

At the onset of anthesis when flowers open, the starch that had accumulated at the base of the 290

stigma is gradually mobilized to support the metabolic activity of the papillae. The papillae are 291

cells with finger-like projections located atop the stigma whose function is to synthesize and 292

release a multitude of different secretions including mucilages, pectins (Edlund et al., 2004), 293

arabinogalactan proteins (AGP) (Lee et al., 2008), and oils (Konar and Linskens, 1966) which 294

combine to facilitate adhesion, hydration, and germination of pollen grains. Flowers with dry 295

stigmas still secrete polymers in the cleft underneath the cuticle (Clarke et al., 1977). The material 296

secreted by the papillae forms the “foot” that anchors the pollen grain and creates the hydrophilic 297

microenvironment which attracts water and germinating factors toward the pollen. Cytological 298

examinations of stigmas from diverse plant species revealed the presence of cells with dense 299

cytoplasm, numerous mitochondria, ER, and Golgi vesicles, which are notable signs of an intense 300

metabolic activity (Rosen and Thomas, 1970; Labarca and Loewus, 1972; Elleman et al., 1992). 301

Direct evidence of stigma active metabolism has been provided by experiments performed with 302

radioactively labeled sugars and amino acids. Indeed, when detached styles of lily flowers were 303

provided with labeled glucose, inositol, and proline, radioactivity was revealed in the sugars 304

(galactose, rhamnose, and arabinose) secreted by the stigma, as well as in the carbohydrates that 305

composed the cell wall of pollen grains germinated on top of those (Labarca et al., 1970). 306

Therefore, the stigma not only provides a solid surface where pollen grains can land and adhere 307

but also actively supports pollen germination and the initial phases of pollen tube protrusion. 308

Stigmatic secretion of pectinases and expansins that loosen the cell wall of the grain and ease the 309

protrusion of the tube has also been reported (Boavida et al., 2011). 310

14

The style is symplasmically connected to the flower, however, the strong transcriptional signal of 311

SUC8 and SUC9 transporter genes measured in the cells of the transmitting tissue (Sauer et al., 312

2004) suggests that post-phloem uptake of sucrose is achieved both symplasmically and 313

apoplasmically. The style fulfills similar secreting activity as the stigma (Rosen and Thomas, 314

1970; Sassen, 1974) and in particular, it releases large amounts of AGPs in the extracellular 315

matrix (ECM) through which pollen tubes elongate. AGPs are proteoglycans made of a short 316

chain of dipeptide motifs and a large carbohydrate component that constitutes up to the 90% of 317

the total AGP molecule (Ellis et al., 2010; Knoch et al., 2014). Given that transitory starch stored 318

along the style is also mobilized at anthesis, it most probably provides the backbones for the 319

synthesis of the carbohydrate component of the AGP proteins, although this has not been directly 320

proven. The sugar moiety of the AGPs triggers signaling responses that guide the pollen tube 321

towards the ovule (Dresselhaus and Franklin-Tong, 2013; Jiao et al., 2016). Internalization of 322

AGP carbohydrates by the pollen tube followed by carbohydrates relocation in the callus that 323

pushes the nuclei forward in the direction of pollen tube growth has also been documented (Lee et 324

al., 2009). 325

Symplasmic connections with the ovule are present in the bundle sheet of funiculus and chalaza 326

(Imlau et al., 1999; Werner et al., 2011), where transitory starch also accumulates (Hedhly et al., 327

2016). However, after fertilization, the developing embryo remains symplasmically isolated from 328

the mother tissues and further transport of photoassimilates is attained with specific transporters 329

and carriers (Stadler et al., 2005; Werner et al., 2011; Chen et al., 2015). Here, the expression of 330

SUC1, SUC8, and SUC9 genes has been detected (Sauer et al., 2004; Feuerstein et al., 2010), 331

although differential expression of SUC1 transporter observed in A. thaliana ecotypes suggests 332

functional redundancy. In the ovule, the synergid cells that surround the egg are also 333

metabolically very active. Analysis of transcripts isolated from the synergids of Torenia fournieri 334

revealed that 30% of the transcripts encode cysteine rich proteins (CRP) of the secretory pathway. 335

These include short-distance signaling peptides involved in the sporophytic guidance as for 336

15

example LURE and LORELEI that guide the pollen tube out the transmitting tissue inside the 337

micropyle to fertilize the ovule (Jones-Rhoades et al., 2007; Capron et al., 2008; Okuda et al., 338

2009; Higashiyama and Yang, 2017). After double fertilization, large amounts of sugars are 339

transported to the endosperm where they accumulate as storage reserves for the embryo and are 340

converted to starch, lipids or proteins. As double fertilization marks the beginning of seed and 341

fruit development, we refer to the numerous reviews that have been written on the topic (Weber 342

et al., 1997; Chen et al., 2015; Sosso et al., 2015). Nevertheless, the energy resources still present 343

in the flower (petals, carpel, and filament) are promptly mobilized and repurposed. Indeed, 344

experiments performed with radioactively labeled sucrose applied to senescing daylily flowers 345

revealed that up to 50% of the total sucrose is rapidly and extensively retro-translocated to young 346

developing buds at a rate of 25 cm per hour (Bieleski, 1995; Sklensky and Davies, 2011). 347

Reabsorption of unutilized nectar has also been observed, however, further research on this topic 348

is clearly warranted. 349

350

Finally, it must be remembered that most of the transporters mediating sugar partitioning in 351

flowers have been identified and characterized in studies conducted in model plants such as A. 352

thaliana, N. tabacum and Petunia. While these studies provide a general understanding of the 353

processes occurring in model flowers, different taxa may have evolved slightly different set of 354

transporters and enzymes to distribute sugars among tissues and cells. 355

356

Floral Amino Acids: Synthesis and Function 357

Assimilation of inorganic nitrogen (N) into organic compounds takes place primarily in the root 358

where ammonium is initially incorporated into glutamine, asparagine, glutamate, and aspartate 359

(Coruzzi, 2003; Näsholm et al., 2009). Then, amino acids and small peptides are loaded into the 360

vasculature of xylem and phloem and transported to sink organs. In flowers, symplasmic and 361

apoplasmic partitioning of organic N follows the routes previously described for sugars 362

16

distribution. Similarly, the transport of amino acids and small peptides across the plasma 363

membrane of tissue symplasmically isolated requires the assistance of protein carriers. In fact, 364

numerous amino acids transporters are expressed in pollen, which is symplasmically isolated 365

from the remaining part of the flower (Foster et al., 2008). Current knowledge on amino acids 366

transporters (Rentsch et al., 2007; Tegeder, 2012) and their expression and function in flowers 367

(Tegeder and Rentsch, 2010) has been compiled in recent reviews. Therefore, we refer to those 368

for a detailed description of floral transporters and provide an overview of the sites of their 369

expression in Figure 2. In this section, we focus on the more recent discoveries regarding the 370

synthesis and physiological functions of amino acids that take place in flowers. 371

In flowers, amino acids are utilized as building blocks for the synthesis of enzymes and structural 372

proteins, as well as precursors of N-containing secondary metabolites and signaling molecules. 373

Despite the common belief that amino acids are exclusively transported to flowers from roots and 374

leaves, evidence has emerged that their de novo synthesis also occurs in floral tissues. For 375

example, studies conducted in petals of Petunia initially aimed to characterize the enzymatic 376

reactions for the production of benzenoid volatile compounds brought to the identification of the 377

enzymes prephenate amino transferase (PPA-AT) and arogenate dehydratase (ADT1) of the 378

phenylalanine biosynthetic pathway. The plastidial CATION AMINO ACID PHE 379

TRANSPORTER (PhpCAT) was also identified in these studies (Maeda et al., 2010; Maeda et 380

al., 2011; Maeda and Dudareva, 2012; Widhalm et al., 2015), as well as the cytosolic 381

phenylalanine biosynthetic pathway (Yoo et al., 2013). Phylogenetic studies revealed that these 382

enzymes and transporters are also present in plants that produce negligible amounts of aromatic 383

volatile compounds, where they may provide the phenylalanine that is incorporated into floral 384

enzymes and structural proteins. 385

Recently, it was shown that the asparagine biosynthetic pathway is also active in flowers. Indeed, 386

asparagine synthetase 1 (ASN1) encoding for the enzyme that transfers amide N from glutamine 387

to asparagine releasing asparagine and glutamate, displays a high level of expression in flowers. 388

17

ASN1 transcription increases throughout the lifespan of A. thaliana flowers, starting from the 389

stages that precede anthesis, up to pollination and early embryo growth (Le et al., 2010). 390

Concomitantly, genes of the asparagine metabolism are also upregulated and floral asparagine 391

content also rises (Gaufichon et al., 2017). Having a high nitrogen-to-carbon ratio (2 N to 4 C), 392

asparagine is an efficient carrier and storage compound of N. Thus, enhancing the supply of 393

asparagine during flower development is an effective strategy to store reserves that will be used 394

to generate energy during ovule maturation and embryo growth (Gaufichon et al., 2017). In 395

developing pollen grains, hydrolysis of asparagine by asparaginase A1 and B1 (ASPGA1 and 396

ASPGB1) releases ammonium, which is later re-assimilated into glutamine, the precursor for the 397

synthesis of other amino acids (Ivanov et al., 2012; Guan et al., 2014). 398

De novo synthesis of proline also occurs in flowers. Proline is found as a free amino acid in 399

pollen grains and nectar, and as a component of proteins of the pollen coat (Lamport et al., 2011; 400

Biancucci et al., 2015). Free proline in pollen grains is thought to act as an osmotic protectant 401

towards desiccation (Chiang and Dandekar, 1995), while proline in nectar may serve as a 402

propellant for the lift phase of flight of insect pollinators (Carter et al., 2006). In addition to the 403

transcriptional activation of the floral proline transporter (Schwacke et al., 1999), high levels of 404

proline in flower are obtained via upregulation of the pyrroline-5-carboxylate synthetase (P5CS) 405

enzyme, which catalyzes the conversion of glutamate to pyrroline-5-carboxylate (Kishor et al., 406

2015). Interestingly, proline is the most abundant amino acid in nectar regardless of the 407

evolutionary distance between plant species (Carter et al., 2006; Nepi et al., 2012). This suggests 408

that proline may have a relevant ecological role for rewarding animal pollinators (Carter et al., 409

2006). 410

As we briefly mentioned above, amino acids and small peptides are synthesized in large amounts 411

by the cells of the transmitting tissue and ovule. These include numerous small secreted proteins 412

of unknown function (Jones-Rhoades et al., 2007) and cysteine-rich proteins such as the LUREs, 413

which are involved in the female gametophytic guidance of pollen tube attraction (Okuda et al., 414

18

2009; Takeuchi and Higashiyama, 2012; Higashiyama and Yang, 2017). -Amino butyric acid 415

(GABA), a non-proteinogenic amino acid that contributes to pollen tube growth and attraction is 416

also produced in the cells of the transmitting tissue. GABA is synthesized in the cytosol by the 417

activity of GABA glutamate decarboxylase and degraded in the mitochondria by the activity of 418

the GABA transaminase (Fait et al., 2008), the latter being encoded by the POLLEN-PISTIL 419

INCOMPATIBILITY 2 (POP2) gene. The coordinated activity of glutamate decarboxylase and 420

transaminase along the pistil creates a gradient of GABA concentration that guides the pollen 421

tube towards the ovule. The disruption of this gradient observed in the pop2 mutants negatively 422

influences the success of fertilization (Palanivelu et al., 2003). 423

424

425

Chemical Modifications of Nectar by Colonizing Microorganisms 426

A large proportion of floral primary metabolites is channeled into the nectar, which is a water-427

based secretion of sugars, amino acids, lipids and secondary metabolites including VOCs. The 428

ecological function of nectar is to reward animal pollinators, therefore, its chemical composition 429

differs among plant species as it evolved to enhance floral visitation by pollinators and reduce the 430

losses imposed by nectar thieves and florivores (Nicolson and Thornburg, 2007). In the last 431

decade, research on nectar had seen a renaissance brought about by targeted nectary 432

transcriptomics and metabolomics (Kram et al., 2009; Noutsos et al., 2015), and the discovery of 433

the mechanisms regulating nectar secretion such as transporters (Lin et al., 2014), hormones 434

(Wiesen et al., 2016), and transcription factors (Liu et al., 2009). These recent discoveries on 435

nectar biology have been compiled in exhaustive reviews (Nepi, 2017; Roy et al., 2017). Hence, 436

we exclusively focus discussion here on the chemical modifications of nectar primary metabolites 437

that are induced by floral microbes. 438

Inoculation of floral nectar with yeasts, bacteria, and fungi takes place during floral visitation by 439

pollinators and florivors (Belisle et al., 2012; Anderson et al., 2013; Aleklett et al., 2014). Given 440

19

this horizontal transfer from the animals to the flowers, the epiphytic communities of microbes of 441

the anthosphere differ from the microbial species of rhizosphere and phyllosphere. Moreover, in a 442

single flower, organ-specific species of microbes separately grow on sepals, petals, and nectaries 443

(Junker et al., 2011; Aleklett et al., 2014). The microbial communities that colonize the 444

anthosphere depend upon the combinatorial effects of plant genotype and the ability of the 445

microbes to competitively exploit the carbon and nitrogen resources present in floral tissues and 446

exudates (Junker and Keller, 2015; Pozo et al., 2016). Without any doubt, nectar offers an ideal 447

habitat to support microbial growth, with sugars providing the substrate for microbial 448

fermentation and amino acids contributing required nitrogen. That microorganisms can modify 449

the composition of nectar became evident when the uniformity of nectar sugar content from 450

plants grown in a glasshouse contrasted with the variability of field-grown plants of the same 451

species (Canto et al., 2007). 452

Yeasts are the most common group of microbes found in flowers, with individuals of the genus 453

Metschnikowia being predominant (Pozo et al., 2016). Following yeast inoculation, sucrose-454

dominant nectar shows a shift towards fructose or glucose that is proportional to the rate of 455

microbial growth (Herrera et al., 2008; de Vega and Herrera, 2013). This implies that yeast cells 456

hydrolyze sucrose to fructose and glucose, but then preferentially utilize one of the two hexoses. 457

Lastly, highly concentrated sucrose-dominant nectar (typically dry nectar) prevents yeast growth 458

(Schaeffer et al., 2015). 459

Floral bacteria received far less attention than yeasts, until pyrosequencing and culturing 460

techniques made it possible to identify the strains that grow on flowers (Fridman et al., 2012; 461

Junker and Keller, 2015). Similarly to yeast, bacterial growth also negatively correlates with total 462

sugar content and/or sucrose content in nectar, but usually positively correlates with the 463

proportion of the monosaccharide fructose (Vannette et al., 2013; Lenaerts et al., 2016; Vannette 464

and Fukami, 2016). In addition, bacterial isolates of the genus Acinetobacter can convert sucrose 465

into a mucous matrix of polysaccharides (Fridman et al., 2012) (Fig. 1F). 466

20

Although the chemical modifications of nectar by yeasts and bacteria look very similar, the 467

effects on pollinators' preferences frequently diverge. The presence of bacterial colonies on floral 468

nectar often has negative effects on pollination success (Vannette et al., 2013) and insect 469

visitation rate (Junker et al., 2014). Conversely, nectar inoculated with yeasts results in increased 470

seed set of bumblebee- and hummingbird-pollinated flowers (Vannette et al., 2013), as well as 471

enhanced pollen donation via increment of pollinator foraging rate (Schaeffer and Irwin, 2014). 472

Nectar modifications of the amino acids content represent a small and under investigated field of 473

research. However, early observations suggest that bacteria may cause a reduction of specific 474

amino acids such as threonine and valine (Lenaerts et al., 2016). 475

476

477

Primary metabolites and pollinators’ preferences: implications for seed and fruit set 478

Seeds and fruits develop following a successful process of plant reproduction, which ultimately 479

depends upon the proper development of the stamen and pistil coupled to successful pollination 480

and fertilization events. Since floral primary metabolism is deeply intertwined with flower 481

development, aberrant floral metabolism can form a prezygotic barrier that prevents mating and 482

fertilization. For example, mutations that impair the metabolic processes of pollen and eggs 483

maturation, or interfere with pollen germination, tube growth and guidance (both in the pollen 484

and in the transmitting tissue) impede pollination and fertilization. As detrimental as these 485

mutations seem to be, they are favorably exploited in agriculture for example in the generation of 486

male sterile plants for hybrid breeding (Goetz et al., 2001; Hirsche et al., 2009). Neither as 487

equally well exploited nor understood, it is the influence that primary metabolism of nectar and 488

pollen has on pollinators’ preferences. Animal-pollinated plants depend upon insects, birds, and 489

mammals as go-betweens for pollen transfer. Therefore, their flowers produce signals (color and 490

scent) to attract pollinators, and nectar and pollen rewards to preserve floral fidelity. However, as 491

animal pollinators display preferences for quality and quantity of the reward, their choice to 492

21

pollinate, or not pollinate a flower affects fertilization and ultimately may reduce seed and fruit 493

set (Hanley et al., 2008; Carruthers et al., 2017). Insect preferences for flower color and odor 494

have been largely investigated and a few studies describe the link between plant genotype and 495

animal behavioral response (Bradshaw Jr and Schemske, 2003; Hoballah et al., 2007; Klahre et 496

al., 2011; Owen and Bradshaw, 2011; Yuan et al., 2013; Amrad et al., 2016; Sheehan et al., 497

2016). Instead, traditional single gene studies to ascertain pollinators’ responses to changes in 498

floral primary metabolism have been delayed by the late discovery of the SWEET9 transporter as 499

a mediator of nectar secretion (Lin et al., 2014), and so far, no transporter has been identified that 500

controls the secretion of amino acids in floral nectar (Zhou et al., 2016). However, a body of 501

growing evidence shows that primary metabolites of pollen and nectar are shaping the interaction 502

between plants and their pollinators through pollination syndromes (Johnson et al., 2006; Weiner 503

et al., 2010). That pollinators’ choices can affect nectar chemical composition was evident since 504

the early studies of Beker (1977) who observed that nectars are richer in amino acids if they are 505

the only source of protein-building material of the pollinators that feed on those. A similar 506

conclusion has been reached in more recent studies which showed that pollinators’ preference had 507

the most important effect on amino acid content in nectar, while taxonomical plant groups had a 508

weakly significant effect (Petanidou et al., 2006). For example, phenylalanine- and GABA-509

enriched nectars are commonly represented in plants pollinated by long-tongued bees and flies 510

independently from their taxonomical group. As GABA functions as an inhibitory 511

neurotransmitter of insects’ nervous system, GABA-rich nectar may be preferred for its calming 512

effect by pollinators (Nepi et al., 2012). Volume of secreted nectar also varies in response to 513

pollinators’ preferences and this happens more rapidly that initially thought. In fact, nectarless 514

plants in bumblebee-pollinated plants appear in a time as short as ten generations (Gervasi and 515

Schiestl, 2017). Pollen chemistry may have a weaker influence on insect preferences as polylectic 516

bees, which collect pollen from plants of different species appear to disregard the chemical 517

composition of pollen despite the beneficial effect that blends of amino acids and polypeptide 518

22

have on colony fitness (Vanderplanck et al., 2014). However, this may not hold true for 519

oligolectic bees, for which pollen chemistry drive evolutionary host-shifts (Vanderplanck et al., 520

2017). These studies and many others present in the literature demonstrate that pollen and nectar 521

chemistry influence pollinators’ choices, but that the interaction is specific between a plant and its 522

pollinators. In addition, it should be considered that very little is known about the transcriptional 523

and post-transcriptional regulation of floral primary metabolism, and how metabolism changes in 524

response to environmental fluctuations (e.g. temperature and rainfall), which may, ultimately, 525

also affect pollination and fertilization success (Gallagher and Campbell, 2017). 526

527

Conclusions and Perspective 528

The current knowledge on flower central metabolism is largely inferred from experiments 529

performed in leaves and it is certainly skewed by the generally accepted prejudice that flowers are 530

entirely heterotrophic. However, we have seen that cycles of carbohydrate hydrolysis and re-531

synthesis are functional and activated in flowers, as well as they are the routes for the 532

biosynthesis of amino acids and peptides. Therefore, there are many unsolved issues concerning 533

floral central metabolism, and the implications for flower development, pollinators’ choices, and 534

seed and fruit set (see Outstanding Questions). The investigations on floral metabolism have 535

certainly been made difficult by the redundant number of transporters of sugars and amino acids 536

which on one side warrant pollination and fertilization success to the plant, but on the other add 537

complexity to a deep understanding of single gene function. In addition, studies performed on 538

knockout mutants focused on the leaf or root phenotypes, and only rarely on flower physiology. 539

Largely under investigated is the measure by which floral metabolism depends on de novo 540

biosynthesis versus intake of sugars and amino acids. There is also a lack of knowledge 541

concerning the spatial distribution of metabolites in floral tissues and their physiological and 542

ecological significance. In addition, analysis of metabolites is often conducted on individual 543

flowers (or inflorescences) that are regarded as integral floral units, despite the fact that in no 544

23

other plant organ as much as in flowers, tissue compartmentalization underlies function. In 545

addition, floral metabolism dramatically changes multiple times in response to development, and 546

presumably, to environmental cues (Lauxmann et al., 2016). Recent advances in analytical 547

techniques that couple metabolomics with histological imaging can now be employed to shed 548

light on this topic (Dong et al., 2016). Techniques of rapid sequencing coupled with genome wide 549

association studies (GWAS) and quantitative trait locus (QTL) analysis promise to speed the 550

discovery rate of genes and the network of genes that control plant-pollinator interactions (Clare 551

et al., 2013; Sedio, 2017). Moreover, with the use of the CRISPR/Cas9 technology the link 552

between a plant genotype, floral chemotype, and pollinator response will likely be possible in 553

non-model organisms. 554

In conclusion, floral biology has become an intense area of study for scientists with expertise in 555

the most disparate disciplines encompassing plant developmental biology, molecular biology, 556

metabolomics and genomics, entomology, and behavioral biology. As described above, recent 557

advances in particular in understanding sugar transport, pollen tube growth, and in better 558

characterizing the chemical composition of nectar provide a firm foundation to comprehend the 559

link between floral metabolism and function. That said, it is our belief that today, as never before 560

a more holistic and collaborative approach is demanded to shed light on the mechanisms that 561

control floral metabolism and the implications for flower development and plant-pollinator 562

interactions. 563

564

565

566

24

Table 1 567

568

Table 1. Overview of the sugar transporters expressed in flowers of Arabidopsis thaliana, organ and tissue of expression, transported substrate, and associated mutant phenotype

SUC, SUCROSE CARRIER, VEX, Vegetative Cell Expressed 1; RPG, Raptured Pollen Grain; VGT, Vacuolar Glucose transporter, INT2, INOSITOL TRANSPORTER; PMT, Polyol/monosaccharide transporter, WT, wild-type, n/a, not available

Name Gene number

Organ (or Tissue) of Expression

Substrate Mutant Phenotype References

SUC1 At1G71880 Stamen, pollen, funiculus (ecotype specific)

sucrose No germination of pollen in absence of sucrose, lower Anthocyanins accumulation

(Sauer and Stolz, 1994; Stadler et al., 1999; Sivitz et al., 2008; Feuerstein et al., 2010)

SUC2/SUT1 At1g22710 Sepals, filament sucrose, maltose, - and -phenylglucoside

Plants are smaller than wild type when grown without sucrose

(Truernit and Sauer, 1995)

SUC3/SUT2 At2G02860 Cerpel, pollen grain and pollen tube

sucrose, maltose n/a (Meyer et al., 2000; Meyer et al., 2004)

SUC4/SUT4 At1G09960 Anthers, pistil, tonoplast sucrose (low affinity transporter) WT (Weise et al., 2000; Schneider et al., 2012)

SUC7/SUT7 At1G66570 Pollen tube growth sucrose Shorter pollen tube growth (ecotype dependent phenotype)

(Johnson et al., 2004; Sauer et al., 2004)

SUC8/SUT8 At2g14670 Transmitting tissue High affinity sucrose; maltose n/a (Sauer et al., 2004)

SUC9/SUT9 At5G06170 Transmitting tissue High affinity sucrose; - and -glucosides, maltose

Early flowering in short day (Sauer et al., 2004; Sivitz et al., 2008)

STP1 At1G11260 Whole flower glucose, galactose, mannose, xylose, 3-O-methylglucose, fructose (traces)

n/a (Sauer et al., 1990)

STP4 At3G19930 Anthers and pollen (expression increases during pollen development)

glucose, galactose, mannose, xylose, 3-O-methylglucose

n/a (Truernit et al., 1996)

STP2 At1G07340 Pollen grains glucose, galactose, mannose, xylose, 3-O-methylglucose, fructose (traces)

n/a (Truernit et al., 1999)

STP6 At3G05960 Pollen (late stages of development)

glucose, galactose, mannose, xylose, 3-O-methylglucose, fructose, ribose

WT (Schneidereit et al., 2003)

25

STP9 At1G50310 Mature pollen, pollen tube glucose, galactose, mannose, xylose n/a (Schneidereit et al., 2003)

STP10 At3G19940 Pollen tube galactose, mannose, glucose WT (Rottmann et al., 2016)

STP11 At5G23270 Pollen tube glucose, galactose, mannose, xylose, 3-O-methylglucose, fructose, ribose

n/a (Schneidereit et al., 2005)

STP13 At5G26340 Sepals, vasculature of emerging petals

glucose, fructose, galactose, mannose WT (Bi et al., 2005; Nørholm et al., 2006)

SWEET1 At1G21460 Pollen grain, pollen tube, petals, sepals

glucose, galactose n/a (Chen et al., 2010)

SWEET2 At3G14770 Sepal, petals, stamen 2-deoxyglucose n/a (Chen et al., 2015)

SWEET3 At5G53190 Stamen 2-deoxyglucose n/a (Chen et al., 2015)

SWEET4 At3G28007 Whole flower, stamen 2-deoxyglucose n/a (Chen et al., 2015)

SWEET5/VEX At5G62850 Pollen (vegetative cells) glucose n/a (Engel et al., 2005)

SWEET7 At4G10850 Stamen glucose n/a (Chen et al., 2015)

SWEET8/RPG1 At5G40260 Pollen grain, pollen tube, tapetum

glucose Male sterility, abnormal microspore membrane, defective exine pattern formation

(Guan et al., 2008; Sun et al., 2013)

SWEET9 At2G39060 Nectary sucrose No nectar secretion (Ge et al., 2000; Lin et al., 2014)

SWEET13/RPG2 At5G50800 Tapetum, tetrad sucrose Male sterility, abnormal microspore membrane, defective exine pattern formation

(Sun et al., 2013)

SWEET14 At4G25010 Stamen sucrose n/a (Chen et al., 2015)

n/a

VGT1 At3G03090 Pollen, (vacuolar transporter)

glucose, fructose Late bolting and flowering (Aluri and Büttner, 2007)

n/a

INT2 At1G30220 tapetum myoinositol and several inositol epimers WT (Schneider et al., 2007)

INT4 At4G16480 Polle, pollen tube, transmitting tissue

myoinositol and several inositol epimers n/a (Schneider et al., 2006)

n/a

26

PMT1 At2g16120 Germinating pollen grains, pollen tube

xylitol, fructose WT (Klepek et al., 2009)

PMT2 At2g16130 Mature pollen grains, pollen tube

xylitol, fructose WT (Klepek et al., 2009)

PMT5/PLT5 At3G18830 Peduncle, sepals, stigma, anthers, abscission zone

ribose, arabinose, xylose, glucose, mannose, galactose, fructose, rhamnose, fucose, sorbotol, erythiol, xylitol, inositol

n/a (Klepek et al., 2005; Reinders et al., 2005)

569

570

27

571

Figure 1. Sugar partitioning in floral tissues. A, Unload of sucrose from the terminal phloem: 572

SUGAR WILL EVENTUALLY BE TRANSPORTED TRANSPORTERS (SWEET) are likely 573

been involved in the process. Cell wall invertase (cwINV) enzymes in the apoplasmic space 574

hydrolyze sucrose to glucose and fructose. SUCROSE TRANSPORTERS (SUTs) alternatively 575

called SUCROSE CARRIERs (SUCs) and SUGAR TRANSPORTER PROTEINS (STPs) carry 576

sucrose and hexose across the plasma membrane of the receptacle cells where carbohydrates are 577

stored as transitory starch. B, In the receptacle, sucrose and hexoses are symplasmically 578

transferred to the anthers. C, cwINVs and sucrose synthases (SUS) hydrolyze sucrose to hexoses, 579

which are transported in the tapetum by SUC/SUT and STP transporters. In the tapetum while it 580

develops, carbohydrates are stored as transitory starch, which is later converted to sucrose by the 581

combined activity of sucrose phosphate synthases (SPS) and sucrose phosphate phosphatase 582

(SPP). D, Pollen grains are apoplasmically isolated and take up sucrose and hexoses via 583

SUC/SUT and STP proteins. In developing pollen grains glucose-6-phosphate is transported 584

across the membrane of amyloplasts by GLUCOSE PHOSPHATE TRANSPORTER 1. Later 585

during development, glucose released by the amyloplasts is internalized in the vacuole by the 586

activity of VACUOLAR GLUCOSE TRANSPORTER 1 (VGT1) and utilized for sucrose 587

synthesis. Depending upon the species, droplets of lipids may also accumulate in mature pollen 588

grains. E, Pollen tube elongation is fuelled by sugars secreted by the transmitting tissue. Hexoses 589

are released in the transmitting tissue by the combined activity of cwINV of pollen grain (♂) and 590

stigma (♀), and by stigma specific vacuolar invertases (VIN). F, SUC/SUT and STP in the cells 591

of the nectary parenchyma take up sucrose and hexoses that are stored as starch granules. Before 592

anthesis, transitory starch is converted to sucrose that is exported by SWEET proteins to the 593

apoplasmic space for nectar secretion. Here, cwINVs hydrolyze sucrose to fructose and glucose. 594

Alternatively, fermentation reactions carried out by colonizing yeasts and bacteria modify the 595

28

sugar composition of nectar by releasing hexoses. Sometimes, the production of a mucous matrix 596

of polysaccharides has also been observed. 597

598

Figure 2. Partitioning of amino acids, amides and peptides in floral tissues. A, In the floral 599

receptacle, transporters of the families of Lysine Histidine Type (LHT), Amino Acid Permease 600

(AAP) and Oligo-Peptide Transporters (OPT) mediate the uptake of neutral (grey circles) and 601

acidic (grey circles with the minus sign) amino acids, neutral and basic (grey circles with the plus 602

sign) amino acids, and tetra- and penta-peptides (purple rectangles), respectively. Expression of 603

the same set of transporters at the base of the ovary suggests that they also mediate the uptake of 604

amino acids and peptides in the ovary. B, In sepals LHT, AAP, OPT, Proline Transporter (ProT) 605

and Cationic Amino acid Transporter (CAT) the latter mediating the transport of both neutral and 606

basic amino acids, are expressed in the cells surrounding the vasculature where they presumably 607

mediate xylem-phloem exchange and/or retrieval of leaked organic nitrogen. C, In petals, 608

plastidial CATs export Phe, Tyr and Trp to the cytoplasm, while Outer Envelope Plastidial 609

protein (OEP) imports amines (N) in the stroma. Mitochondrial Basic Amino acid Carriers 610

(BACs) import Arg in the mitochondrion (mt). Expression of LHT, AAP, OPT, ProT, and CAT 611

was also detected in the cells surrounding petal vasculature. Apoplasmically isolated tissues such 612

as the cells of the tapetum (D), developing pollen grains (E) and pollen tubes (F) express a vast 613

majority of different transporters. PTR-like Peptide Transporter (PTR) in pollen grains and pollen 614

tubes mediate the uptake of de- and tri-peptides. G, In nectar, the pool of amino acids and 615

peptides is depleted by colonizing yeasts and bacteria. 616

617

618

619

620

621

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1092

1093

sucrose

glucose fructose

starch

SWEET

SUC/SUT

STP

PMT

INT

VGT1

yeasts/bacteria

oil polysaccharides

A

B

C

D

E

F

Terminal

Phloem

cwINV

Apoplasm Receptacle Filament

cwINV

B A

amyloplast

Anther Wall Tapetum

C

Loculus Pollen Grain

D

vacuole

amyloplast

Pollen

Tube

Transmitting tissue

E

Nectary parenchyma

F

cwINV

Nectar Apoplasm

amyloplast

cwINV ♂♀

VIN ♀

♂♀ male/female

amyloplast

GPT1

SUS +

UDP

cwINV

UDP

SUS +

UDP

cwINV

UDP

SUS +

UDP

cwINV

UDP

SPS

P

UDP P

SPP + H2O

UDP +

Pi

P

SPS

P

UDP P

SPP + H2O

UDP +

Pi

P

+ Pi

Figure 1. Sugar partitioning in floral tissues. A, Unload of sucrose from the terminal phloem: SUGAR WILL EVENTUALLY BE

TRANSPORTED TRANSPORTERS (SWEET) are likely been involved in the process. Cell wall invertase (cwINV) enzymes in the apoplasmic

space hydrolyze sucrose to glucose and fructose. SUCROSE TRANSPORTERS (SUTs) alternatively called SUCROSE CARRIERs (SUCs)

and SUGAR TRANSPORTER PROTEINS (STPs) carry sucrose and hexose across the plasma membrane of the receptacle cells where

carbohydrates are stored as transitory starch. B, In the receptacle, sucrose and hexoses are symplasmically transferred to the anthers. C,

cwINVs and sucrose synthases (SUS) hydrolyze sucrose to hexoses, which are transported in the tapetum by SUC/SUT and STP

transporters. In the tapetum while it develops, carbohydrates are stored as transitory starch, which is later converted to sucrose by the

combined activity of sucrose phosphate synthases (SPS) and sucrose phosphate phosphatase (SPP). D, Pollen grains are apoplasmically

isolated and take up sucrose and hexoses via SUC/SUT and STP proteins. In developing pollen grains glucose-6-phosphate is transported

across the membrane of amyloplasts by GLUCOSE PHOSPHATE TRANSPORTER 1. Later during development, glucose released by the

amyloplasts is internalized in the vacuole by the activity of VACUOLAR GLUCOSE TRANSPORTER 1 (VGT1) and utilized for sucrose

synthesis. Depending upon the species, droplets of lipids may also accumulate in mature pollen grains. E, Pollen tube elongation is fuelled by

sugars secreted by the transmitting tissue. Hexoses are released in the transmitting tissue by the combined activity of cwINV of pollen grain

(♂) and stigma (♀), and by stigma specific vacuolar invertases (VIN). F, SUC/SUT and STP in the cells of the nectary parenchyma take up

sucrose and hexoses that are stored as starch granules. Before anthesis, transitory starch is converted to sucrose that is exported by SWEET

proteins to the apoplasmic space for nectar secretion. Here, cwINVs hydrolyze sucrose to fructose and glucose. Alternatively, fermentation

reactions carried out by colonizing yeasts and bacteria modify the sugar composition of nectar by releasing hexoses. Sometimes, the

production of a mucous matrix of polysaccharides has also been observed.

Figure 2. Partitioning of amino acids, amides and peptides in floral tissues. A, In the floral receptacle, transporters of the families of Lysine

Histidine Type (LHT), Amino Acid Permease (AAP) and Oligo-Peptide Transporters (OPT) mediate the uptake of neutral (grey circles) and

acidic (grey circles with the minus sign) amino acids, neutral and basic (grey circles with the plus sign) amino acids, and tetra- and penta-

peptides (purple rectangles), respectively. Expression of the same set of transporters at the base of the ovary suggests that they also

mediate the uptake of amino acids and peptides in the ovary. B, In sepals LHT, AAP, OPT, Proline Transporter (ProT) and Cationic Amino

acid Transporter (CAT) the latter mediating the transport of both neutral and basic amino acids, are expressed in the cells surrounding the

vasculature where they presumably mediate xylem-phloem exchange and/or retrieval of leaked organic nitrogen. C, In petals, plastidial CATs

export Phe, Tyr and Trp to the cytoplasm, while Outer Envelope Plastidial protein (OEP) imports amines (N) in the stroma. Mitochondrial

Basic Amino acid Carriers (BACs) import Arg in the mitochondrion (mt). Expression of LHT, AAP, OPT, ProT, and CAT was also detected in

the cells surrounding petal vasculature. Apoplasmically isolated tissues such as the cells of the tapetum (D), developing pollen grains (E) and

pollen tubes (F) express a vast majority of different transporters. PTR-like Peptide Transporter (PTR) in pollen grains and pollen tubes

mediate the uptake of de- and tri-peptides. G, In nectar, the pool of amino acids and peptides is depleted by colonizing yeasts and bacteria.

A

D

E

F

G

A

LHT

ProT

AAP

OPT

BAC

OEP

PTR

CAT

neutral amino acids

basic amino acids +

acidic amino acids -

amine

yeasts/bacteria

Pro

Phe/Tyr/Trp

peptide

Loculus Pollen Grain

E

B

C

Apoplasm Receptacle Ovary

- -

Petal Vasculature

-

C mt

Arg

+ +

+ -

+ + -

Sepal

B

Vasculature

- -

+ +

+ - -

+

+ - +

-

Anther Wall Tapetum

D

- -

+ +

-

- +

+

-

+

-

+

Pollen

Tube

Transmitting tissue

F G

Nectar

- - -

+ +

+ +

+

-

-

-

-

plastid

plastid

mt

Arg

N ..

N ..

N ..

N ..

N ..

ADVANCES

• The functional coupling of cwINV of the pollen

tube and transmitting tissue supports tube

elongation and successful fertilization.

• The sugar moiety of AGPs enables pollen

response to LURE.

• Asparagine synthesis in flowers is supported by

ASN1, which provides asparagine for embryo

development.

• SWEET9 regulates nectar secretion.

OUTSTANDING QUESTIONS

• In which measure is floral central metabolism

self-sustained or supported by carbon and

nitrogen fluxes from source tissues?

• How is floral central metabolism

transcriptionally and posttranscriptionally

regulated?

• What is the influence of environmental cues on

floral central metabolism and how does this

influence flower-pollinator interactions and

ultimately fruit and seed yield?

• What regulates the secretion of amino acids and

proteins into nectar?

• How do developmental changes in the

metabolism of one floral organ influence the

metabolism of others?

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