Does abiotic stress cause functional B vitamin deficiency? · ... D.R.M) and Food Science and Human...

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Short title: B Vitamin Deficiency and Abiotic Stress 1

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Corresponding author: Andrew D. Hanson, [email protected] Phone (352) 273-4856 3

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Research Area: Topical Reviews (Associate Editor Julia Bailey-Serres) 5

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Does abiotic stress cause functional B vitamin deficiency in plants? 7 8

Andrew D. Hanson, Guillaume A. Beaudoin, Donald R. McCarty, and Jesse F. Gregory III 9

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Horticultural Sciences Department (A.D.H., G.A.B., D.R.M) and Food Science and Human Nutrition 11

Department (J.F.G.), University of Florida, Gainesville, FL 32611-0690, USA 12

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One-sentence Summary: 15

Unlike animals, plants produce their own B vitamins but may nonetheless suffer vitamin deficiencies 16

under stress conditions, with wide-ranging metabolic consequences. 17

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Author contributions: 20

A.D.H. conceived the article and wrote the manuscript along with G.A.B., D.R.M., and J.F.G. 21

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Funding information: 23

This work was supported by National Science Foundation award IOS-1444202. 24

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Corresponding author: Andrew D. Hanson [email protected] 26

Plant Physiology Preview. Published on November 2, 2016, as DOI:10.1104/pp.16.01371

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Abstract 27

B vitamins are the precursors of essential metabolic cofactors, but are prone to destruction under 28

stress conditions. It is therefore a priori reasonable that stressed plants suffer B vitamin deficiencies, 29

and that certain stress symptoms are metabolic knock-on effects of these deficiencies. Given the 30

logic of these arguments, and the existence of data to support them, it is a shock to realize that the 31

roles of B vitamins in plant abiotic stress have had minimal attention in the literature (100-fold less 32

than hormones) and continue to be overlooked. In this article, we therefore aim to explain the 33

connections among B vitamins, enzyme cofactors, and stress conditions in plants. We first outline 34

the chemistry and biochemistry of B vitamins, and explore the concept of vitamin deficiency with the 35

help of information from mammals. We then summarize classical and recent evidence for stress-36

induced vitamin deficiencies and for plant responses that counter these deficiencies. Lastly, we 37

consider potential implications for agriculture. 38 39 Key Words: Biotin, folate, niacin, pantothenate, pyridoxine, riboflavin, thiamin 40

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INTRODUCTION 42

The great pioneers of modern plant physiology pointed out that B vitamins have much in common 43

with hormones, and even classified some vitamins as plant hormones (i.e. plant growth regulators in 44

today’s terms) (Went et al., 1938; Bonner and Bonner, 1948; Thimann, 1963). In plants, as in anim-45

als, B vitamins and hormones are biologically active in minute amounts, are transported, and lead to 46

similarly profound consequences when deficient (Bonner and Bonner, 1948). B vitamins and 47

hormones might consequently be expected to have received comparable research attention. This 48

has broadly been the case in biomedical research since vitamins and hormones were first 49

discovered (Kohler, 1975). It has almost never been the case in any area of plant research, including 50

abiotic stress. Thus, in the Arabidopsis abiotic stress literature, articles involving hormones 51

outnumber those involving B vitamins by a factor of 100 (Supplemental Table S1). 52 53 This stunning disparity suggests two things about past and present thinking in the abiotic stress field. 54

First, it indicates a prevalent default assumption that the whole of B vitamin metabolism always and 55

everywhere continues to work well in stressed plants – and so can be safely ignored. Second, and 56

relatedly, it signals a lack of attention to the possibility that stress-induced defects in B vitamin meta-57

bolism can be intermediate causes of system-wide plant stress responses. Neither the default ass-58

umption nor the inattention is reasonable a priori and they are not justified by the available evidence. 59 60 This review sets out to show that B vitamin deficiency is a simple, probable, but overlooked scenario 61

in abiotic stress responses. We begin by providing key background information on the chemical and 62

metabolic lability of B vitamins and the cofactors derived from them, and on the concept of vitamin 63



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deficiency derived from work in animals. We then revisit classical studies that point clearly to roles 64

for B vitamins in abiotic stress, but are no longer in the modern canon, and assess recent evidence 65

for such roles. Next, we outline how plants combat stress-induced B vitamin deficiencies. Lastly, we 66

consider how understanding stress-induced vitamin deficiency could inform crop breeding and 67

management. 68 69 Two points should be made at the outset. First, there has been much research on the B vitamin con-70

tents of food plants and on B vitamin synthesis and metabolism in plants. However, the main – if not 71

sole – driver for this valuable work has been plants as vitamin sources for humans rather than plants 72

as vitamin sources for themselves (Fitzpatrick et al., 2012; Gerdes et al., 2012). This article takes 73

the complementary position that ‘plants need their vitamins too’ (Smith et al., 2007). Second, re-74

search on vitamin C (ascorbate) shows that plant stress biology does not invariably sideline vitamins 75

(Foyer and Noctor, 2011). This article argues that B vitamins deserve as much attention as vitamin 76

C. 77

78

CHEMICAL AND METABOLIC LABILITY – WHY BAD THINGS HAPPEN TO GOOD VITAMINS 79

B vitamins are indispensable because they are the metabolic precursors of essential cofactors. Fig-80

ure 1 shows the seven B vitamins found in plants, along with the cofactors to which they are 81

converted. In brief: Thiamin (vitamin B1) is converted to thiamin diphosphate; riboflavin (vitamin B2) 82

to flavin mononucleotide (FMN) and flavin adenine dinucleotide (FAD); niacin (vitamin B3) to 83

NAD(P)+; pantothenate (vitamin B5) to coenzyme A and the prosthetic group of acyl carrier protein; 84

pyridoxine (vitamin B6) to pyridoxal 5'-phosphate; biotin (vitamin B8) to the biotinyl side-chain of 85

enzymes; and tetrahydrofolate (historically termed vitamin B9) to various one-carbon substituted 86

folates and their polyglutamylated derivatives. 87 88 Cofactors function by participating in biochemical reactions, e.g. thiamin diphosphate forms covalent 89

complexes with carbonyl substrates, FAD and NAD(P)+ become reduced as substrates are oxidized, 90

and coenzyme A forms thioesters with acyl groups. Cofactors and their vitamin precursors are thus 91

chemically reactive by nature. Their chemically reactive groups are therefore prone to undergo spon-92

taneous side-reactions such as oxidation, hydrolysis, racemization, or addition that damage or des-93

troy the molecule – and stress conditions promote such side-reactions (Piedrafita et al., 2015). For 94

example, most abiotic stresses cause accumulation of reactive oxygen species (You and Chan, 95

2015) that can inflict oxidative damage on every compound in Figure 1. Similarly, temperature extr-96

emes, high light levels, pH excursions, and stress-driven accumulations of metabolites with which 97

cofactors react all directly accelerate diverse types of spontaneous cofactor damage (e.g. Treadwell 98

and Metzler, 1972; Baggott, 2000; Mills et al., 2006; Marbaix et al., 2011). Abiotic stresses can also 99

promote cofactor damage indirectly by altering compartmentation (e.g. Akhtar et al., 2010; Moham-100



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madi et al., 2012), by inducing enzymes that break down cofactors (e.g. Rapala-Kozik et al., 2008; 101

Higa et al., 2012), and by creating harsh cellular conditions in which enzymes that normally act on 102

other substrates become more promiscuous (Piedrafita et al., 2015) and mistakenly attack cofactors. 103 104 Figure 1 uses color-coded arrows to show the site and nature of damage reactions that vitamins and 105

cofactors can undergo in physiological conditions, and Table I catalogs the reactions corresponding 106

to the arrows. Note that Figure 1 is bristling with arrows – which helps explain why most of the B 107

vitamins/cofactors made it into a ‘Top 30’ list of damage-prone metabolites (Lerma-Ortiz et al., 2016) 108

and why all organisms have dedicated systems to deal with vitamin/cofactor damage (Linster et al, 109

2013). “Bad things happen” to B vitamins and cofactors because these compounds are basically 110

chemical and metabolic “accidents waiting to happen”. Also, unlike many other reactive metabolites, 111

cofactors are end-products, not short-lived intermediates that are quickly converted to something 112

else. The longer an end-product lives, the higher the probability of its getting damaged at some point. 113 114 Thiamin diphosphate deserves special mention for metabolic lability because, unlike other cofactors, 115

it can be damaged during the catalytic cycle (‘catalysis-induced inactivation’) (McCourt et al., 2006). 116

Oxygen-dependent side-reactions in enzyme active sites convert the thiamin diphosphate cofactor to 117

an inactive thiazolone derivative (Sümegi and Alkonyi, 1983; Bunik et al., 2007). Such use-depend-118

ent damage explains why thiamin is the only B vitamin whose dietary requirement in animals is pro-119

portional to non-fat energy intake (McCourt et al., 2006). More generally, the damage reactions un-120

dergone by all B vitamins account for their dietary requirements; if vitamins were not continuously 121

damaged they would last forever and not need to be constantly resupplied. In this context it is note-122

worthy that the whole-body half-life of thiamin (and its phosphates) in humans is one to two orders of 123

magnitude shorter than those of other B vitamins for which estimates are available, as follows: thia-124

min, 9.5–18.5 days (Ariaey-Nejad et al., 1970); folates, 60–150 days (Gregory and Quinlivan, 2002); 125

vitamin B6, ~500 days (Coburn, 1990); vitamin B12 (absent from plants), 480–1284 days (Hall, 1964). 126

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WHAT ACTUALLY CONSTITUTES B VITAMIN DEFICIENCY? 128

The concept of vitamin deficiency comes from human and animal nutrition; it refers to the consequ-129

ences of a shortfall in the dietary supply of a specific vitamin. Because plants make their own B 130

vitamins, and indeed are the ultimate source of most of the B vitamins consumed by animals, the 131

concept of ‘B vitamin deficiency’ might seem inapplicable to plants, and hence irrelevant. But, as we 132

will show, this concept is very relevant to plants. 133 134 Key questions about B vitamin nutrition in animals are: ‘What dietary intake of each vitamin is 135

needed for optimal growth and health?’ and ‘What happens when the supply of a vitamin falls below 136

the optimal level?’ Both questions are often answered by measuring weight gain in young animals 137



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given various vitamin doses in the diet, and by tracking levels of the vitamin and its corresponding 138

cofactor in tissues and organs. Figure 2 (left half) summarizes data from such studies, in which 139

various levels of thiamin, pyridoxine, or folate were supplied to rats whose growth and liver cofactor 140

levels were monitored. Two points that emerge from these data are: (i) There is a continuum rather 141

than a sharp divide between vitamin sufficiency and deficiency; and (ii) the cofactor level in liver 142

does not have to fall much before growth is substantially impacted (as are development, metabolic 143

functions, and behavior, not shown), and declines of 30–60% from optimal are devastating. Animals 144

therefore operate their vitamin and cofactor systems with rather narrow margins of safety. 145 146 The same appears to be true of plants. Nutritional trials analogous to those above have not yet been 147

conducted using totally vitamin-deficient mutants. However, mutant plants partially deficient in thi-148

amin or vitamin B6 have been studied (Woodward et al., 2010; Rueschhoff et al., 2013), as have cult-149

ured cells depleted in folate using a reasonably specific antifolate drug (Loizeau et al., 2008) (Fig. 2, 150

right half). Although these experiments produced a single deficient state, not a range as in rats, the 151

data clearly suggest that a 25–40% loss of cofactor leads to severe consequences. To summarize: 152

The red zone on the B vitamin fuel gauge seems to be in roughly the same place in plants and 153

animals, and is quite close to the full mark. 154 155 A subsidiary concept within vitamin deficiency is ‘functional vitamin deficiency’, wherein vitamin and 156

cofactor measurements need not show marked depletion but strong metabolic disturbances never-157

theless ensue. A prime example is vitamin B12 (absent from plants), whose deficiency in humans is 158

better diagnosed by its metabolic consequences (elevated levels of methylmalonic acid and homo-159

cysteine) than by measuring B12 itself (Stabler et al., 1996). Another example is folate, for which – in 160

contrast to B12 – deficiency causes elevation only of homocysteine and not of methylmalonic acid 161

(Green, 2008). Functional deficiencies of other B vitamins in humans generally affect enzymes hav-162

ing the weakest affinity for their cofactor relative to the cofactor’s intracellular concentration, as is the 163

case for vitamin B6 (Ueland et al., 2015). However, the hierarchy of biochemical reactions most sus-164

ceptible to deficiency of B vitamins has not been fully clarified. 165 166 Functional vitamin deficiencies also can arise when the deficiency occurs in a particular (inaccess-167

ible) tissue or compartment but does not affect the whole organism – or at least the part convenient 168

for assessing vitamin or cofactor status. Such a situation could develop in roots for thiamin and 169

niacin because roots of certain species import these vitamins from shoots (Bonner and Bonner, 170

1948). Intracellular deficiencies are also possible given that B vitamins and cofactors are synthes-171

ized and used in different compartments. For example, thiamin diphosphate is made in the cytosol 172

but used mainly in plastids and mitochondria (Rapala-Kozik et al., 2012), and vitamin B6 is made in 173

the cytosol but used throughout the cell (Fitzpatrick et al., 2011). In this connection, note that the 174



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plastids of the vitamin B6 deficient Arabidopsis mutant in Figure 2 were far more severely deficient in 175

B6 than the leaf as a whole (Rueschhoff et al., 2013), and that a thiamin-requiring tobacco mutant 176

appeared to suffer primarily from thiamin deficiency in chloroplasts (McHale et al., 1988). 177

178

EVIDENCE FOR STRESS-INDUCED B VITAMIN DEFICIENCY 179

The previous sections explained that B vitamins and cofactors are chemically and metabolically un-180

stable, that stresses potentially make them even more unstable, and that modest falls in cofactor 181

levels slow growth. We might therefore predict that (i) abiotic stresses cause vitamin and cofactor 182

deficiencies, (ii) the deficiencies degrade plant performance, and (iii) supplementing stressed plants 183

with the deficient vitamin(s) improves performance. Evidence from both classical and modern work 184

indicates that all these things happen. 185

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Classical Evidence 187

The classical evidence was considered in a short 1957 article with the evocative title ‘The chemical 188

cure of climatic lesions’ (Bonner, 1957). The idea captured in the title was that negative effects of 189

‘climatic lesions’ (i.e. physicochemical environmental stresses) could be ‘cured’ by applying vitamins 190

or other essential metabolites, singly or in mixtures. ‘Chemical cures’ by B vitamins were reported for 191

various plants and various abiotic stresses during the 1940s–1960s; typical data are shown in Figure 192

3. In each case, applying a vitamin or vitamin mixture promoted growth in unfavorable conditions but 193

not in favorable ones. These results are de facto confirmation that stress can lead to functional B 194

vitamin deficiency. Importantly, the Arabidopsis work in Figure 3 gave stress-induced vitamin defic-195

iency a genetic basis by defining ecotypic differences attributable to one or a few genes (Langridge 196

and Griffing, 1959). This is the pattern expected if the enzymes that use a particular cofactor bind to 197

that cofactor with different strengths. When the vitamin starts to run out and cofactor levels fall, the 198

weakest binder loses activity first, and small allelic differences in the affinity of this enzyme for the 199

cofactor become critical determinants of performance of the organism as a whole (Guenther et al., 200

1999). 201

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Modern Evidence 203

Although the exogenous application approach (‘spray and pray’) has fallen out of fashion, it can be 204

perfectly valid, and beneficial effects of applying B vitamins – particularly thiamin – to stressed crop 205

species continue to be reported, e.g. for salinized wheat, sunflower, and maize (Al-Hakimi and 206

Hamada, 2001; Sayed and Gadallah, 2002; Tuna et al., 2013; Kaya et al., 2015). Also, a rigorous 207

Arabidopsis study showed that thiamin enhances tolerance to oxidative stress imposed by paraquat 208

(Tunc-Ozdemir et al., 2009). Such protective effects of thiamin on stressed plants are generally 209

interpreted in terms of the antioxidant properties of thiamin and its diphosphate (Lukienko et al., 210



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2000), but the in-vivo relevance of these properties has been questioned (Lesgards et al. 2015) and 211

it is not clear that the observed protection is due to direct antioxidant effects (Asensi-Fabado and 212

Munné-Bosch, 2010). The experimental data are equally compatible with the protection being due to 213

relief of a functional deficiency of thiamin diphosphate and the consequent restoration of normal 214

metabolic fluxes. Although bias from prior positive reports may be at work, it is interesting that thia-215

min features so prominently in the literature on vitamin application, given that thiamin and thiamin di-216

phosphate are particularly labile in vivo (see above). It is also interesting in the light of the extremely 217

high energetic cost and inefficiency of thiamin biosynthesis (Box 1), to which we will return later. 218 219 Further modern support for stress-induced deficiency of four different B vitamins has come from mol-220

ecular genetics, as follows. (i) Pyridoxine: The Arabidopsis SOS4 (SALT OVERLY SENSITIVE 4) 221

gene for pyridoxal kinase was cloned via the salt-sensitive phenotype of sos4 mutants, which was 222

reverted by pyridoxine (Shi et al., 2002) – a textbook ‘cure’ of a stress lesion. Arabidopsis mutants in 223

the PDX1.3 gene for pyridoxal 5'-phosphate synthase were found to be hypersensitive to salt, 224

osmotic, and oxidative stress (Chen and Xiong, 2005; Titiz et al., 2006). (ii) Pantothenate/coenzyme 225

A: The Arabidopsis HAL3A (HALOTOLERANCE DETERMINANT 3A) gene, first identified for its relat-226

ion to stress tolerance (Espinosa-Ruiz et al., 1999), was shown to code for a key enzyme in panto-227

thenate conversion to coenzyme A (Kupke et al., 2001), and HAL3A overexpression increased salt 228

tolerance (Espinosa-Ruiz et al., 1999; Yonamine et al., 2001). (iii) Folate: Ablation of the Arabidopsis 229

gene encoding a cytosolic folate synthesis enzyme (HPPK/DHPS) specifically impacted salt and 230

oxidative stress-resistance at germination (Storozhenko et al., 2007; Navarrete et al., 2012). (iv) 231

Riboflavin: The Arabidopsis phs1 (PHOTOSENSITIVE 1) mutant, first identified by its sensitivity to 232

high-light stress (Ouyang et al., 2010), was found to lack a functional domain of the riboflavin 233

biosynthesis enzyme PyrR (Hasnain et al., 2013; Frelin et al., 2015). Note the pattern here: Either a 234

gene identified via a stress-sensitive phenotype turned out to be a B vitamin or cofactor synthesis 235

enzyme, or ablating a known B vitamin/cofactor enzyme caused stress sensitivity. 236

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COUNTERING STRESS-INDUCED B VITAMIN DEFICIENCY 238

Conceptually, resource deficiencies can be countered by (1) maintaining and then mobilizing re-239

serves, (2) obtaining more of the resource, (3) repairing or recycling it, or (4) using less of it. Plants 240

certainly deploy strategies 2 and 3 to confront B vitamin deficiency, and potentially deploy the others. 241 242 Strategy 1: Storing and Mobilizing B Vitamins and Precursors 243

Storage forms of B vitamins have had little attention in the plant literature, in sharp contrast to stor-244

age forms of hormones (Ludwig-Müller, 2011; Piotrowska and Bajguz, 2011). Storage forms of vit-245

amins and vitamin precursors – mainly glucosides and glucose esters – nevertheless exist and some 246

can reach higher concentrations than the corresponding free forms (Gregory, 1998). The only B vita-247



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min for which no storage forms have been reported is thiamin. Storage forms have not been analyz-248

ed in abiotic stress studies, perhaps because they are not commercially available as standards. Un-249

fortunately, this means that the contribution of storage forms to B vitamin homeostasis during stress 250

remains unresolved; this contribution could, however, be large. The main storage forms are shown in 251

Figure 4 and described below, starting with the two vitamins (B6 and B3) whose storage forms are 252

reported to be more abundant than the free forms in certain species and tissues. 253 254 Pyridoxine (B6). The 5'-β-D-glucoside of pyridoxine, and other glycosides linked via the 4- or 5-hydr-255

oxymethyl groups, can contribute up to 75% of the total vitamin B6 in plant tissues (Gregory, 1998), 256

i.e. they can be the largest item in the B6 budget. A glucosyltransferase responsible for pyridoxine-5'-257

β-D-glucoside synthesis has been detected in pea (Tadera et al., 1982); enzymatic hydrolysis of the 258

glucoside has been shown in vitro (Yasumoto et al., 1976) so it can presumably be mobilized in vivo. 259 260 Niacin (B3). Nicotinic acid-N-β-D-glucoside and N-methylnicotinate (trigonelline) are widespread in 261

plants and can be major metabolites of nicotinamide and nicotinate (Matsui et al., 2007; Ashihara et 262

al., 2010); more complex glycosides also occur (Gregory, 1998). Enzymes that would allow the N-263

glucoside and trigonelline to act as mobilizable storage forms have been characterized (Upmeier et 264

al., 1988; Shimizu and Mazzafera, 2000; Mizuno et al., 2014). Brassicaceae contain the β-D-glucosyl 265

ester of nicotinic acid, which almost certainly acts as a mobilizable storage form (Li et al., 2015). 266 267 Pantothenate (B5). Pantothenate 4'-O-β-D-glucoside has been isolated from tomato fruit (Amachi et 268

al., 1971) and is most likely present in a wide range of species and tissues (Yoshizumi and Amachi, 269

1969). Glycosides of the lactone form of pantoate, the immediate precursor of pantothenate (pant-270

oyllactone-β-D-glucopyranoside and pantoyllactone primeveroside) occur in rice seedlings, the lev-271

els in coleoptile tissue being in the millimolar range (Menegus et al., 2002). These pantoate derivat-272

ives seem not to have been sought in any plant besides rice; they could conceivably be widespread. 273 274 Tetrahydrofolate Precursors. The precursor p-aminobenzoate was converted to its β-D-glucosyl 275

ester by all tissues and species tested and was found to be the major endogenous form of p-amino-276

benzoate (Quinlivan et al., 2003). The esterification reaction is reversible and the ester is stored in 277

vacuoles (Eudes et al., 2008). Glycosides (probably β-D-glucosides) of the tetrahydrofolate precurs-278

ors neopterin and monapterin were found in tomato fruit engineered to overproduce pterins (Díaz de 279

la Garza et al., 2004); it is not known whether such glycosides occur naturally, or whether they can 280

be mobilized. 281 282 Riboflavin (B2). The α and β forms of riboflavin-5′-D-glucoside have been found in germinating barl-283

ey seedlings supplied with riboflavin (Suzuki and Uchida, 1983). As with the pterin glycosides above, 284

it is it is not known whether riboflavin glucosides occur naturally, or whether they can be mobilized. 285 286



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Biotin (B7). While no small-molecule conjugates of biotin have been reported, a biotinyl protein that 287

represents >90% of the total protein-bound biotin has been characterized and cloned from pea 288

seeds (Dehaye et al., 1997), and is conserved among higher plants (Gerdes et al., 2012). 289 290 Strategy 2: Increasing B Vitamin Supply 291

Many analyses of gene and protein expression have indicated that abiotic stresses upregulate flux 292

through some but not all B vitamin biosynthesis pathways and studies of the effects of stress on the 293

levels of vitamins and cofactors tend to support this inference. As is usual in stress research, 294

differences in experimental design (the species and tissue used, the timing, duration, and severity of 295

stress, the analysis methods applied – blots/microarrays/RNAseq, etc) preclude meta-analysis of all 296

the data. Below, we therefore focus first on a high-throughput dataset – the AtGenExpress global 297

stress expression dataset (available at http://jsp.weigelworld.org/expviz/expviz.jsp) – supplemented 298

with broadly comparable data from several independent Arabidopsis stress studies (Supplemental 299

Table S2). We then highlight illustrative papers on pyridoxine and thiamin. 300 301 Note that even when a vitamin biosynthetic pathway is clearly upregulated in response to stress, 302

stress-induced vitamin or cofactor deficiency may still occur for several reasons. Firstly, activating 303

biosynthetic gene expression may fail to increase vitamin production due to downstream constraints, 304

e.g. the energy cost of making THI4 protein for thiamin biosynthesis (see below and Box 1). Sec-305

ondly, as noted above, a high vitamin or cofactor status – as measured in whole organs, tissues, or 306

cells – can obscure functional deficiencies within sub-compartments. Lastly, conversion of vitamins 307

to cofactors may become limiting, so that increases in vitamin levels do not always result in higher 308

cofactor levels. Cofactor levels can consequently fall even when free vitamin levels rise – and cofact-309

or levels – not vitamin levels – determine metabolic outcomes. 310 311 Arabidopsis Gene Expression. The stresses used for the AtGenExpress global stress expression 312

dataset (heat, cold, drought, salt, high osmolarity, UV-B light, and wounding) were essentially single-313

regime shock treatments, lasting 24 hours or less, given to Arabidopsis seedlings (Kilian et al., 314

2007); the protocols in the other studies listed in Supplemental Table S2 were quite similar. The 315

transcriptional responses observed in these experiments therefore necessarily only included part of 316

the plant’s full repertoire. These responses nonetheless follow the coherent pattern seen in Figure 5, 317

a bird’s-eye schematic of B vitamin synthesis and salvage pathways in which enzymes are 318

represented by rectangles. The color density of each enzyme is proportional to the number of differ-319

ent stresses that induce the corresponding gene by two-fold or more. The pathways are arranged in 320

order of prevalence of gene induction. At one extreme (biotin, pantothenate/CoA, and tetrahydro-321

folate pathways) just one or two biosynthetic genes are induced by a single stress, whereas at the 322

other extreme (vitamin B6 and thiamin pathways) all the known biosynthetic genes are induced by at 323



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least three stresses. Except for B6, the prevalence of induction of salvage genes basically tracks that 324

of biosynthetic genes. This overview of gene-level data thus indicates that certain B vitamin biosyn-325

thesis pathways – particularly those for B6 and thiamin – are upregulated by several abiotic stresses 326

and that others – such as the tetrahydrofolate pathway – are largely not. Vitamin/cofactor analysis 327

data and protein-level data for vitamin B6 and thiamin are consistent with this picture, as discussed 328

next. 329 330 Vitamin B6. Pyridoxal 5′-phosphate is made by the pyridoxal synthase complex, which consists of 331

two proteins, PDX1 and PDX2 (the two red-colored boxes in the pyridoxal 5′-phosphate section of 332

Figure 5). Arabidopsis has three PDX1 homologs, of which PDX1.1 and PDX1.3 are active enzymes 333

and PDX1.2 is a positive regulator (Titiz et al., 2006; Moccand et al., 2014). Paralleling the stress 334

induction of Arabidopsis PDX genes (Fig. 5; Supplemental Table S2), PDX1.3 protein accumulated 335

and the total B6 level increased by 60% in response to UV-B exposure (Ristilä et al., 2011); total B6 336

also increased by 60% in response to heat stress (Moccand et al., 2014). Levels of pyridoxal 5'-337

phosphate and free pyridoxal or pyridoxine likewise increased by about two-fold in tobacco exposed 338

to chilling, UV radiation, osmotic stress, oxidative stress, or drought (Huang et al., 2013). 339 340 Thiamin. Thiamin is synthesized by a pathway that is very energetically expensive because the thi-341

azole moiety is made by a suicide enzyme (THI4), and the pyrimidine moiety is made by a radical 342

SAM (S-adenosylmethionine) enzyme (THIC) that probably lasts for only a few catalytic cycles (Box 343

1). Paralleling the stress induction of Arabidopsis THI4, THIC, and other thiamin synthesis genes 344

(Fig. 5; Supplemental Table S2), the level of total thiamin and of its components (thiamin mono- and 345

diphosphates and free thiamin) increased by up to two-fold in Arabidopsis seedlings subjected to 346

cold, osmotic, salinity, or oxidative stress (Tunc-Ozdemir et al., 2009). Similarly, total thiamin 347

increased by up to 60% in Arabidopsis seedlings exposed to salt, osmotic, or oxidative stress, with 348

free thiamin contributing as much or more than thiamin diphosphate to the increase (Rapala-Kozik et 349

al., 2012). Also similarly, in maize seedlings subjected to water, salt, or oxidative stress, total thiamin 350

increased by 70-150%, due to increases in free thiamin and thiamin monophosphate (Rapala-Kozik 351

et al., 2008). However, in this case levels of the cofactor thiamin diphosphate stayed constant or fell 352

by up to 30%, which is quite enough to cause severe deficiency symptoms (Fig. 2) and illustrates the 353

point made above about cofactor levels falling even though free vitamin levels rise. 354 355 Given the suicide nature of the THI4 enzyme, it is striking that THI4 was the most highly or second 356

most highly induced gene in cotton seedlings exposed to cold, drought, salt, or high pH stress; the 357

induction of THI4 relative to unstressed controls ranged from 14-fold to 44-fold (Zhu et al., 2013). It 358

is equally striking that the THI4 protein showed, among all proteins analyzed, the second largest 359



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increase in expression (3.2-fold) in heat-stressed poplar leaves (Ferreira et al., 2006) and the third 360

largest increase in expression (3.7-fold) in heat-stressed wild rice leaves (Scafaro et al., 2010). 361 362 Strategy 3: Repairing or Recycling Damaged B Vitamins and Cofactors 363

Like other organisms, plants have enzyme systems that deal with some of the chemical and enzym-364

atic damage reactions shown in Figure 1 (Linster et al., 2013). These enzyme systems may repair 365

damaged vitamins and cofactors, i.e. directly restore them to the original state, or salvage parts of 366

damaged molecules for re-use in biosynthesis. As vitamin and cofactor repair (Hanson et al., 2016) 367

and recycling (Gerdes et al., 2012) were recently reviewed, we focus here on three cases where the 368

repair or recycling-related activity appears to be upregulated by stress and not simply constitutive. 369 370 Thiamin Salvage Hydrolase TenA_E. TenA_E mediates two successive steps in the recovery of 371

the pyrimidine moiety from thiamin damaged in the thiazole moiety (Zallot et al., 2014). The Ara-372

bidopsis gene encoding TenA_E is upregulated by several abiotic stresses, in common with thiamin 373

synthesis genes (Fig. 4; Supplemental Table S2). The Arabidopsis gene specifying the thiazole 374

salvage enzyme ThiM (Yazdani et al., 2013) is not upregulated (Fig. 4), which fits with the thiazole 375

moiety of thiamin being more prone to irreversible damage than the pyrimidine moiety, and hence 376

not as recyclable (Zallot et al., 2014). 377 378 Thiamin Diphosphate-related Nudix Hydrolases. These enzymes (NUDT20 and NUDT24 in Ara-379

bidopsis) are diphosphatases whose preferred substrates are damaged – and toxic – forms of thiam-380

in diphosphate, including the previously mentioned thiazolone form generated by oxygen-dependent 381

side-reactions (Goyer et al., 2013). The diphosphatase reaction is both a detoxification step and the 382

first step in salvage of the pyrimidine moiety. The Arabidopsis gene(s) (which are not distinguished 383

by microarrays) are induced between two-fold and five-fold by salt, drought, and osmotic stress, and 384

probably also oxidative stress (Kilian et al., 2007; Goyer et al., 2013). 385 386 NAD(P)+ Salvage Module. Two enzymes mediating consecutive steps in NAD(P)+ salvage (nicotin-387

amidase and nicotinate phosphoribosyltransferase) are each induced by two stresses in Arabidopsis 388

(Fig. 5), as is a transporter (NiaP) for nicotinate, the intermediate that these enzymes share (Kilian et 389

al., 2007). Arabidopsis NiaP also transports trigonelline (Fig. 4) (Jeanguenin et al., 2012). NiaP is 390

probably located in the plasma membrane (Jeanguenin et al., 2012), suggesting that nicotinate salv-391

aged in one location could be re-used for NAD(P)+ synthesis in another. This would be consistent 392

with the classical evidence for inter-organ exchange of nicotinate (Bonner and Bonner, 1948). 393

394

Strategy 4: Decreasing Demand for B Vitamins 395

Metabolism can sometimes be re-routed to bypass certain cofactor-dependent steps, as in the phos-396

phate starvation response, in which alternative bypass pathways of cytosolic glycolysis are upregul-397



12

ated to spare scarce adenylates and phosphate (Plaxton and Tran, 2011). There are as yet no cases 398

of full-blown re-routing in response to vitamin deficiency, although two studies provide indirect evi-399

dence for redirection of fluxes that may be, at least in part, active responses. In the first study, 400

tobacco leaves overexpressing transketolase, a thiamin diphosphate-dependent enzyme, became 401

moderately thiamin diphosphate-deficient, and showed reduced isoprenoid synthesis via the thiamin 402

diphosphate-dependent enzyme 1-deoxy-D-xylulose 5-phosphate synthase (DXS); this reduction 403

was associated with lower DXS transcript levels (Khozaei et al., 2015). In the second study, a 404

drastic, rapid-onset tetrahydrofolate deficiency in Arabidopsis cells treated with antifolate drugs led 405

to initial depletion of methionine and S-adenosylmethionine pools, reflecting reduction in the tetra-406

hydrofolate-dependent flux of one-carbon units to methionine as one-carbon fluxes were adaptively 407

reprioritized in favor of nucleotides (Loizeau et al., 2007). Surprisingly, the methionine and S-aden-408

osylmethionine pools – and by inference the associated fluxes – subsequently returned to normal, in 409

part via a conserved adaptive mechanism, triggered by tetrahydrofolate deficiency, that involves 410

proteolytic removal of the N-terminal regulatory region of the methionine synthesis enzyme 411

cystathionine γ-synthase (Loizeau et al., 2007). 412

413

AGRICULTURAL IMPLICATIONS 414

As Abraham Blum has emphasized (Blum, 2014), humility and caution are needed when trying to 415

predict agricultural benefits by extrapolating from the responses of seedlings of Arabidopsis or other 416

species to short, sharp stresses in growth chambers (which describes most of the experiments cov-417

ered above). With this warning in mind, what might stress-induced B vitamin and cofactor deficiency 418

imply for crop breeding and management? The primary implication is that breeding for enhanced vit-419

amin content (biofortification) – by transgenic or other approaches – could pay off in terms of stress-420

resistance as well as human nutrition (Fitzpatrick et al., 2012). If stress indeed predisposes to defic-421

iency, a clear prescription for stress-resistance breeding would be: ‘Keep your cofactors safe’. 422 423 The two B vitamins most connected with stress responses, vitamin B6 and thiamin (Fig. 5), are 424

targets of transgenic biofortification efforts in Arabidopsis (Raschke et al., 2011; Pourcel et al., 2013; 425

Vanderschuren et al., 2013; Dong et al., 2015), and stress tests have been run on the engineered 426

plants, albeit mainly with plantlets cultured on agar medium containing sucrose (i.e. not photo-427

synthesizing normally). The total B6 content of leaf tissue was boosted up to four-fold, and included 428

large increases in the cofactor pyridoxal 5'-phosphate and pyridoxine-5'-β-D-glucoside (Raschke et 429

al., 2011). The total thiamin content of leaf tissue was boosted up to 3.4-fold, contributed by up to 430

two-fold increases in the cofactor thiamin diphosphate and up to six-fold increases in thiamin (Dong 431

et al., 2015). The B6-biofortified plants were larger than controls and more resistant to paraquat-432

imposed oxidative stress; no other stress data were reported (Raschke et al., 2011). The thiamin-433



13

fortified plants showed no change in resistance to salt, cold, osmotic, drought, or oxidative stress 434

(Dong et al., 2015). To summarize: These first biofortification results for B6 and thiamin are incon-435

clusive and merit follow-up. 436 437 Stress-induced B vitamin deficiency also has implications for crop management (Plaut et al., 2013). 438

Reported benefits of vitamin applications are cited above; such applications are most likely to be 439

useful in practice if they can be given as seed-priming treatments (Al-Hakimi and Hamada, 2001), 440

i.e. applied to seed before sowing. Such seed treatments are cost-efficient (Tanou et al., 2012). 441

442

FUTURE PERSPECTIVES 443

The preceding overview of work relating B vitamins to abiotic stress raises five issues that are listed 444

in the Outstanding Questions Box. Each issue is developed briefly below 445 446 Itemizing Stress-relevant Enzyme Reactions. Although various enzymes and genes for repair or 447

recycling of damaged vitamins and cofactors are known, this is still not the case for about half of the 448

30 damage reactions in Figure 1. While the products of some of these reactions may have no 449

possible fate besides complete degradation, comparative biochemistry suggests that others may 450

well be reclaimed in plants; examples include biotin sulfoxide and chain-shortened biotin (Linster et 451

al., 2013), pyridoxine and nicotinamide N-oxides (Sakuragi and Kummerow, 1960; Shibata et al., 452

1991), and riboflavin-4',5'-phosphate (cyclic FMN) (Fraiz et al., 1998). Nor do we know most of the 453

enzymes or genes for the synthesis and mobilization of the vitamin conjugates in Figure 4, and it is 454

not even clear that we have fully inventoried the conjugates that plants can make. Notably, conjug-455

ated forms of thiamin and its pyrimidine and thiazole precursors have not been reported from plants, 456

but they seem not to have been sought. 457 458 Graduating to Crops and Realistic Stress. As noted previously, most of the modern data linking 459

abiotic stress with B vitamins and cofactors comes from young Arabidopsis plants and unrealistic 460

stress protocols. This is a generic weakness of molecular-level stress research, and the resulting 461

disconnect from agriculture goes a long way toward explaining why molecular work has had a very 462

limited impact on breeding for stress environments (Blum, 2014). It is consequently important to 463

extend stress/vitamin work from Arabidopsis to good genetic model crops such as tomato, canola, 464

maize, and rice, and to adopt stress protocols that mimic field stresses to plants beyond the seedling 465

stage. 466 467 Diagnosing Functional Deficiencies. Vitamin deficiencies, particularly functional ones affecting on-468

ly certain cells or compartments, may be better diagnosed from characteristic changes in metabolite 469

profiles than by directly measuring vitamin levels, as discussed above for vitamin B12 deficiency in 470

humans (Stabler et al., 1996). Given the possibility that direct vitamin measurements can fail to 471



14

detect subtle but physiologically critical functional deficiencies, and the high cost and low-throughput 472

nature of many vitamin assays, indirect assessment of plant vitamin and cofactor status via metabol-473

omics is appealing. Confirming or disconfirming the validity of this approach in plants, as in humans 474

(Stabler et al., 2013), will require prior metabolic profiling studies of vitamin-deficient mutants. An 475

alternative indirect, high-throughput way to detect functional vitamin deficiencies may be via charact-476

eristic transcriptome changes, analogous to the induction of specific genes by mineral nutrient defic-477

iencies (e.g. Nikiforova et al., 2003; Zheng et al., 2009). Furthermore, transcriptome analysis could 478

uncover mechanisms that re-route metabolism to mitigate the effects of vitamin deficiency (see 479

above). Again, evaluation of these possibilities will require studies of vitamin-deficient mutants. 480

481

Genotypic Variation. Although there is natural genotypic variation in vitamin content (Hanson and 482

Gregory, 2011; Fitzpatrick et al., 2012), it would be impractical to use vitamin content as a selection 483

criterion to develop experimental populations due to the issues of assay cost and efficacy just outlin-484

ed. On the other hand, were high-throughput indirect methods to assess deficiency available (see 485

above), it would be feasible to assess vitamin/cofactor status in populations subjected to realistic 486

stresses, and then to work back via genome-wide association studies to genes governing 487

vitamin/cofactor status. Once identified, such genes, which would presumably include known and 488

novel genes with repair/recycling, synthesis, storage, or bypass functions, could be used to explore 489

a ‘keep your cofactors safe’ breeding strategy for abiotic stress resistance. 490 491 Is Thiamin an Achilles’ Heel in Stress Metabolism? A thread running through the whole of this re-492

view is that thiamin and thiamin diphosphate are not like the other B vitamins and cofactors. Thiamin 493

diphosphate may turn over exceptionally fast, at least in part because of its unusual feature of 494

catalytic inactivation. Thiamin is energetically costly to make due to the suicidal nature of one of its 495

biosynthetic enzymes and the suicidal tendency of another. Because thiamin synthesis depends 496

absolutely on concurrent protein synthesis it is vulnerable to stress in a way that other B vitamins are 497

not. Unlike most other B vitamins, thiamin and its precursors lack known storage forms. Thiamin 498

synthesis and salvage genes are particularly highly stress-regulated in Arabidopsis seedlings. And 499

lastly, thiamin is more prominent than other B vitamins in the ‘spray and pray’ literature. Taken 500

together, these features suggest that thiamin could be an Achilles’ heel – a crucial weak point – in 501

plant stress metabolism. 502

503

Supplemental Data 504

The following supplemental materials are available. 505

• Supplemental Table S1. Analysis of Arabidopsis stress literature based on PubMed search 506

terms. 507



15

• Supplemental Table S2. Stress-induced B vitamin/cofactor synthesis and salvage genes in 508

Arabidopsis. 509

510

ACKNOWLEDGMENTS 511

We apologize to the authors of relevant studies that could not be cited here due to page limitations, 512

and thank Dr. Claudia Lerma Ortiz for a helpful critique of a draft of the review. 513

514



16

515

Box 1. Thiamin Biosynthesis – A High-cost, High-risk Operation 516

Enzymes all have finite lifespans, but some have much shorter lifespans than others. These include 517

so-called ‘suicide enzymes’ in which a residue is irreversibly altered after just one turnover, as well 518

as enzymes employing reactive radicals as intermediates, e.g. radical S-adenosylmethionine (SAM) 519

enzymes, which typically catalyze fewer than a dozen turnovers in vitro (Broderick et al., 2014). 520

Enzymes with short lifespans are energetically costly because they have to be replaced so often. 521 522 Thiamin is much more energetically costly to produce than other vitamins because its first biosynth-523

etic enzymes, THI4 and THIC, have extremely short lifespans. THI4 (also called THI1) synthesizes 524

the thiazole moiety of thiamin (Figure). The sulfur atom in the thiazole ring comes from a conserved 525

cysteine in THI4 whose loss permanently inactivates the protein, making THI4 a suicide enzyme 526

(Chatterjee et al., 2013). THIC synthesizes the pyrimidine moiety of thiamin. THIC is a radical SAM 527

enzyme that may achieve no more than five catalytic turnovers in vitro (Palmer and Downs, 2013). 528

Thus THI4 and THIC mediate orders of magnitude fewer catalytic events during their lives than most 529

other enzymes. 530 531 This catalytic inefficiency is manifested in vivo. In proteomic analyses of barley leaves, the THI4 and 532

THIC proteins had, respectively, the first and fifth highest turnover rates of more than 500 proteins 533

studied (Nelson et al., 2014). The half-lives of THI4 and THIC were just a few hours compared to 534

days for most proteins. 535 536 Another consequence may be high vulnerability of the thiamin biosynthetic pathway to stress. Global 537

responses to abiotic stress include shutting down protein synthesis in general (Dhindsa and Cleland, 538

1975; Good and Zaplachinski, 1994) and specifically inducing proteins involved in protein folding and 539

processing (Liu and Howell, 2010). Such reprioritization could adversely impact the replacement of 540

THI4 and THIC, without which thiamin synthesis cannot proceed. 541

542

Box 1 Figure. Catalytic longevity and protein turnover in thiamin synthesis. The number of catalytic 543

turnovers that each pathway enzyme mediates during its lifetime (represented by the width of the 544

blue reaction arrows) varies from thousands to <10 for THIC and one for THI4. The consequent 545

rapid turnover of the THIC and THI4 proteins is schematized by red arrows. Abbreviations: AIR, 546

aminoimidazole ribotide; HET, hydroxyethylthiazole, HMP, hydroxymethylpyrimidine, P, phosphate, 547

PP, diphosphate. 548

549



17

550

Advances Box 551

● Recent research and the classical literature on ‘the chemical cure of climatic lesions’ converge to 552

indicate that stressed plants can develop functional B vitamin deficiencies. 553

● Fully appreciating the lability and metabolic centrality of B vitamins and cofactors makes clear that 554

they are crucial stress-sensitive nodes in pathway networks that cells must seek to protect. 555

● Protection strategies include repairing or recycling damaged vitamins and cofactors, increasing 556

biosynthesis by upregulating biosynthetic gene expression, and probably mobilizing reserves. 557

● Thiamin is the most metabolically labile B vitamin and the only one whose synthesis depends on 558

suicidal enzymes, implying that thiamin pools are doubly difficult to maintain in stress conditions. 559

560

561

Outstanding Questions Box 562

● Have we documented all the relevant metabolic reactions of B vitamins and cofactors? 563

● Do the results from model stresses in Arabidopsis apply to realistic stresses in crops? 564

● Can functional B vitamin deficiency be diagnosed from metabolome/transcriptome changes? 565

● How far can genotypic variation in vitamins or cofactors explain variation in stress resistance? 566

● Is thiamin really the most stress-sensitive B vitamin? 567

568



18

FIGURE LEGENDS 569

570

Figure 1. Structures and damage reactions of the seven B vitamins found in plants and of repres-571

entative cofactors derived from them. The vitamin moieties are highlighted in blue. Note that folates 572

generally have a short γ-linked polyglutamate chain attached to the glutamyl moiety. Color-coded 573

arrows show the site and nature of spontaneous chemical or enzymatic damage reactions that each 574

vitamin/cofactor can undergo in vivo. The damage reactions involved are documented in Table I. 575

576

Figure 2. Comparing growth responses to deficiencies of thiamin, B6, or folate in rats versus plants. 577

The decline from vitamin sufficiency to deficiency is approximated by a color gradient. For rats, 578

deficiencies were obtained by varying dietary vitamin content; liver was used to assess vitamin 579

status. For plants, the experiments involved vitamin deficient mutants (blk-1 for thiamin in maize, 580

pdx1.3 for B6 in Arabidopsis) or cell cultures treated with an antifolate drug for folate in Arabidopsis. 581

Whole plants, leaves, or cells were used to assess vitamin status. Data sources: rat thiamin, Rains 582

et al. (1997); rat B6, Mackey et al. (2003) and Scheer et al. (2005); rat folate, Clifford et al. (1993); 583

maize thiamin, Woodward et al. (2010); Arabidopsis B6, Rueschhoff et al. (2013); Arabidopsis folate, 584

Loizeau et al. (2008). 585

586

Figure 3. Classical data on the chemical cure of high- or low-temperature growth lesions. Day/night 587

temperatures are in ºC. +, Vitamin(s) added; – , no vitamin; differences significant at * P <0.05, ** P 588

<0.01. The data are for species of the ornamental plant Cosmos (Bonner, 1943), for Arabidopsis 589

(Langridge and Griffing, 1959), and for other species (Ketellapper, 1963). 590

591

Figure 4. Structures of conjugated forms of B vitamins and their precursors that occur in plants. The 592

molecules to which the vitamins and precursors are conjugated are colored blue. 593

594

Figure 5. Stress induction of B vitamin and cofactor synthesis and salvage genes in Arabidopsis. 595

Synthesis and salvage pathways for each vitamin are schematized as in Gerdes et al. (2012) except 596

for the omission of compartmentation and the addition of two thiamin salvage reactions (Yazdani et 597

al., 2013; Zallot et al., 2014). Circles are metabolites, arrows are reactions, and rectangles are 598

enzymes. The full pathway schemes, which include enzyme and metabolite names, are available at 599

http://pubseed.theseed.org/seedviewer.cgi?page=PlantGateway. Enzymes whose genes are induc-600

ed at least two-fold by 0, 1, 2, or ≥3 different abiotic stresses (in shoots or roots) are color coded 601

white and three shades of red, respectively. Gene expression data were taken from AtGenExpress 602

and literature summarized in Supplemental Table S2. 603

604



19

Table I. Chemical and enzymatic damage reactions of B vitamins and the corresponding cofactors

Vitamin/cofactor Reactions C/Ea Referencesb

Thiamin (vitamin B1) Thiamin diphosphate

Pyrimidine ring deamination Thiazole ring oxidation Thiazole ring breakdown Oxidation to thiamin acetate Hydrolysis to thiazole + pyrimidine Dephosphorylation Thiamin triphosphate formation

C C,E C E E E E

Windheuser and Higuchi, 1962 Bunik et al., 2007; Dwivedi and Arnold, 1973 Jenkins et al., 2007 Dalvi et al., 1974 Jurgenson et al., 2009 Rapala-Kozik et al., 2009 Linster et al., 2013

Riboflavin (vitamin B2) FMN, FAD

(Photo)oxidative flavin ring loss (Di)phosphate bond hydrolysis 7α- and 8α-hydroxylation Cyclic FMN formation from FAD

C E E

C,E

Choe et al., 2005 Ogawa et al., 2008; Rawat et al., 2011 Ohkawa et al., 1983 Pinto et al., 1999; Sánchez-Moreno et al. 2009

Niacin (vitamin B3) NAD(P)(H)

Hydration of nicotinamide ring Epimerization of β- to α-NAD(P)H Hydrolytic loss of nicotinamide ring Diphosphate bond hydrolysis Nicotinamide ring addition reactions

C,E C E E C

Marbaix et al., 2011 Oppenheimer and Kaplan, 1975 Everse et al., 1975 Ogawa et al., 2008 Everse et al., 1971

Pantothenate (vitamin B5) Coenzyme A, ACPc

Oxidations of the thiol group Diphosphate bond hydrolysis Hydrolysis of the 3' phosphate group

C E E

Huang et al., 2016 Ogawa et al., 2008 Paizs et al., 2008

Pyridoxine (vitamin B6) Pyridoxal 5'-phosphate

Aldehyde group oxidation Aldehyde group condensations Dephosphorylation 6-Hydroxylation

C/E C E C

Gerdes et al., 2012 Dalling et al., 1976 Gerdes et al., 2012 Tadera et al., 1986

Biotin (vitamin B8) Biotinylated enzymes

Oxidation to biotin sulfoxide Side chain β-oxidation

C E

Melville, 1954 Izumi et al., 1973

Tetrahydrofolate C1-Substituted folates

Oxidative cleavage of C9-N10 bond Pteridine ring oxidation 5-Formyltetrahydrofolate formation γ-Glutamyl bond hydrolysis

C C/E C/E E

Gregory, 1989 Noiriel et al., 2007 Baggott, 2000; Goyer et al., 2005 Orsomando et al., 2005; Bozzo et al., 2008

605 aC, chemical (i.e. non-enzymatic, spontaneous) reaction; E, enzymatic reaction or side-reaction. 606 bCertain reactions have so far been reported only from animals or microbes. cACP, acyl carrier protein, which has a bound 4'-phosphopantetheinyl prosthetic group derived from coenzyme A.

607

608

609



20

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http://www.ncbi.nlm.nih.gov/pubmed?term=Dalling DK%2C Grant DM%2C Horton WJ%2C Sagers RD %281976%29 Carbon 13 NMR study of nonenzymatic reactions of pyridoxal 5%27%2Dphosphate with selected amino acids and of related reactions%2E J Biol Chem 251%3A 7661%2D7668&dopt=abstract

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Good AG, Zaplachinski ST (1994) The effects of drought stress on free amino acid accumulation and protein synthesis in Brassicanapus. Physiol Plant 90: 9-14


Goyer A, Collakova E, Díaz de la Garza R, Quinlivan EP, Williamson J, Gregory JF 3rd, Shachar-Hill Y, Hanson AD (2005) 5-Formyltetrahydrofolate is an inhibitory but well tolerated metabolite in Arabidopsis leaves. J Biol Chem 280: 26137-26142


Goyer A, Hasnain G, Frelin O, Ralat MA, Gregory JF 3rd, Hanson AD (2013) A cross-kingdom Nudix enzyme that pre-empts damagein thiamin metabolism. Biochem J 454: 533-542


Green R (2008) Indicators for assessing folate and vitamin B12 status and for monitoring the efficacy of intervention strategies.Food Nutr Bull 29: S52-S63


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Paizs C, Diemer T, Rétey J (2008) The putative coenzyme B12-dependent methylmalonyl-CoA mutase from potatoes is aphosphatase. Bioorg Chem 36: 261-264


Palmer LD, Downs DM (2013) The thiamine biosynthetic enzyme ThiC catalyzes multiple turnovers and is inhibited by S-adenosylmethionine (AdoMet) metabolites. J Biol Chem 288: 30693-30699


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http://www.ncbi.nlm.nih.gov/pubmed?term=Nelson CJ%2C Alexova R%2C Jacoby RP%2C Millar AH %282014%29 Protein with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling%2E Plant Physiol 166%3A 91%2D108&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nikiforova V%2C Freitag J%2C Kempa S%2C Adamik M%2C Hesse H%2C Hoefgen R %282003%29 Transcriptome analysis of sulfur depletion in Arabidopsis thaliana%3A interlacing of biosynthetic pathways provides response specificity%2E Plant J 33%3A 633%2D650&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ogawa T%2C Yoshimura K%2C Miyake H%2C Ishikawa K%2C Ito D%2C Tanabe N%2C Shigeoka S %282008%29 Molecular char�acterization of organelle%2Dtype Nudix hydrolases in Arabidopsis%2E Plant Physiol 148%3A 1412%2D1424&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ohkawa H%2C Ohishi N%2C Yagi K %281983%29 New metabolites of riboflavin appear in human urine%2E J Biol Chem 258%3A 5623%2D5628&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Oppenheimer NJ, Kaplan NO (1975) The alpha beta epimerization of reduced nicotinamide aden�ine dinucleotide. Arch Biochem Biophys 166: 526-535

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http://www.ncbi.nlm.nih.gov/pubmed?term=Orsomando G%2C de la Garza RD%2C Green BJ%2C Peng M%2C Rea PA%2C Ryan TJ%2C Gregory JF 3rd%2C Hanson AD %282005%29 Plant gamma%2Dglutamyl hydrolases and folate polyglutamates%3A characterization%2C com�part�mentation%2C and co%2Doccurrence in vacuoles%2E J Biol Chem 280%3A 28877%2D28884&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ouyang M%2C Ma J%2C Zou M%2C Guo J%2C Wang L%2C Lu C%2C Zhang L %282010%29 The photosensitive phs1 mutant is impaired in the riboflavin biogenesis pathway%2E J Plant Physiol 167%3A 1466%2D1476&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Paizs C%2C Diemer T%2C R�tey J %282008%29 The putative coenzyme B12%2Ddependent methylmalonyl%2DCoA mutase from potatoes is a phosphatase%2E Bioorg Chem 36%3A 261%2D264&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Paizs C, Diemer T, R�tey J (2008) The putative coenzyme B12-dependent methylmalonyl-CoA mutase from potatoes is a phosphatase. Bioorg Chem 36: 261-264

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Paizs&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Palmer LD%2C Downs DM %282013%29 The thiamine biosynthetic enzyme ThiC catalyzes multiple turnovers and is inhibited by S%2Dadenosylmethionine %28AdoMet%29 metabolites%2E J Biol Chem 288%3A 30693%2D30699&dopt=abstract

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Rapala-Kozik M, Golda A, Kujda M (2009) Enzymes that control the thiamine diphosphate pool in plant tissues. Properties ofthiamine pyrophosphokinase and thiamine-(di)phosphate phosphatase purified from Zea mays seedlings. Plant Physiol Biochem47: 237-242


Rapala-Kozik M, Kowalska E, Ostrowska K (2008) Modulation of thiamine metabolism in Zea mays seedlings under conditions ofabiotic stress. J Exp Bot 59: 4133-4143


Rapala-Kozik M, Wolak N, Kujda M, Banas AK (2012) The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thalianaseedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMCPlant Biol 12: 2


Raschke M, Boycheva S, Crèvecoeur M, Nunes-Nesi A, Witt S, Fernie AR, Amrhein N, Fitzpatrick TB (2011) Enhanced levels ofvitamin B6 increase aerial organ size and positively affect stress tolerance in Arabidopsis. Plant J 66: 414-432


Rawat R, Sandoval FJ, Wei Z, Winkler R, Roje S (2011) An FMN hydrolase of the haloacid dehalogenase superfamily is active inplant chloroplasts. J Biol Chem 286: 42091-42098


Ristilä M, Strid H, Eriksson LA, Strid A, Sävenstrand H (2011) The role of the pyridoxine (vitamin B6) biosynthesis enzyme PDX1 inultraviolet-B radiation responses in plants. . Plant Physiol Biochem 49: 284-292


Rueschhoff EE, Gillikin JW, Sederoff HW, Daub ME (2013) The SOS4 pyridoxal kinase is required for maintenance of vitamin B6-mediated processes in chloroplasts. Plant Physiol Biochem 63: 281-291


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http://search.crossref.org/?page=1&rows=2&q=Plaut Z, Edelstein M, Ben-Hur M (2013) Overcoming salinity barriers to crop production using traditional methods. Crit Rev Plant Sci 32: 250-291

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http://search.crossref.org/?page=1&rows=2&q=Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156: 1006-1015

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http://search.crossref.org/?page=1&rows=2&q=Quinlivan EP, Roje S, Basset G, Shachar-Hill Y, Gregory JF 3rd, Hanson AD (2003) The folate precursor p-aminobenzoate is reversibly converted to its glucose ester in the plant cytosol. J Biol

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http://search.crossref.org/?page=1&rows=2&q=Rains TM, Emmert JL, Baker DH, Shay NF (1997) Minimum thiamin requirement of weanling Sprague-Dawley outbred rats. J Nutr 127: 167-170

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http://search.crossref.org/?page=1&rows=2&q=Rapala-Kozik M, Golda A, Kujda M (2009) Enzymes that control the thiamine diphosphate pool in plant tissues. Properties of thiamine pyrophosphokinase and thiamine-(di)phosphate phosphat�ase purified from Zea mays seedlings. Plant Physiol Biochem 47: 237-242

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http://search.crossref.org/?page=1&rows=2&q=Rapala-Kozik M, Kowalska E, Ostrowska K (2008) Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J Exp Bot 59: 4133-4143


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http://search.crossref.org/?page=1&rows=2&q=Raschke M, Boycheva S, Cr�vecoeur M, Nunes-Nesi A, Witt S, Fernie AR, Amrhein N, Fitzpatrick TB (2011) Enhanced levels of vitamin B6 increase aerial organ size and positively affect stress tolerance in Arabidopsis. Plant J 66: 414-432

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http://search.crossref.org/?page=1&rows=2&q=Ristil� M, Strid H, Eriksson LA, Strid A, S�venstrand H (2011) The role of the pyridoxine (vitamin B6) biosynthesis enzyme PDX1 in ultraviolet-B radiation responses in plants. . Plant Physiol Biochem 49: 284-292

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Yazdani M, Zallot R, Tunc-Ozdemir M, de Crécy-Lagard V, Shintani DK, Hanson AD (2013) Identification of the thiamin salvageenzyme thiazole kinase in Arabidopsis and maize. Phytochemistry 94: 68-73


Yonamine I, Yoshida K, Kido K, Nakagawa A, Nakayama H, Shinmyo A (2004) Overexpression of NtHAL3 genes confers increasedlevels of proline biosynthesis and the enhancement of salt tolerance in cultured tobacco cells. J Exp Bot 55: 387-395


Yoshizumi H, Amachi T (1969) Studies on the bacteria isolated from wine. Part IV. Distribution of the growth factor for a bacteriuminducing malo-lactic fermentation. Agric Biol Chem 33: 18-24


You J, Chan Z (2015) ROS Regulation during abiotic stress responses in crop plants. Front Plant Sci 6: 1092Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zallot R, Yazdani M, Goyer A, Ziemak MJ, Guan JC, McCarty DR, de Crécy-Lagard V, Gerdes S, Garrett TJ, Benach J, Hunt JF,Shintani DK, Hanson AD (2014) Salvage of the thiamin pyrimidine moiety by plant TenA proteins lacking an active-site cysteine.Biochem J 463: 145-155


Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, Shou H (2009) Physiological andtranscriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151: 262-274


Zhu YN, Shi DQ, Ruan MB, Zhang LL, Meng ZH, Liu J, Yang WC (2013) Transcriptome analysis reveals crosstalk of responsivegenes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PLoS One 8: e80218



http://www.ncbi.nlm.nih.gov/pubmed?term=Yazdani M%2C Zallot R%2C Tunc%2DOzdemir M%2C de Cr�cy%2DLagard V%2C Shintani DK%2C Hanson AD %282013%29 Identi�fic�ation of the thiamin salvage enzyme thiazole kinase in Arabidopsis and maize%2E Phytochemistry 94%3A 68%2D73&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yazdani M, Zallot R, Tunc-Ozdemir M, de Cr�cy-Lagard V, Shintani DK, Hanson AD (2013) Identi�fic�ation of the thiamin salvage enzyme thiazole kinase in Arabidopsis and maize. Phytochemistry 94: 68-73

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yonamine I%2C Yoshida K%2C Kido K%2C Nakagawa A%2C Nakayama H%2C Shinmyo A %282004%29 Overexpress�ion of NtHAL3 genes confers increased levels of proline biosynthesis and the enhancement of salt tolerance in cultured tobacco cells%2E J Exp Bot 55%3A 387%2D395&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yonamine I, Yoshida K, Kido K, Nakagawa A, Nakayama H, Shinmyo A (2004) Overexpress�ion of NtHAL3 genes confers increased levels of proline biosynthesis and the enhancement of salt tolerance in cultured tobacco cells. J Exp Bot 55: 387-395

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshizumi H%2C Amachi T %281969%29 Studies on the bacteria isolated from wine%2E Part IV%2E Distribution of the growth factor for a bacterium inducing malo%2Dlactic fermentation%2E Agric Biol Chem 33%3A 18%2D24&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=You J%2C Chan Z %282015%29 ROS Regulation during abiotic stress responses in crop plants%2E Front Plant Sci 6%3A 1092&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=You J, Chan Z (2015) ROS Regulation during abiotic stress responses in crop plants. Front Plant Sci 6: 1092

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http://scholar.google.com/scholar?as_q=ROS Regulation during abiotic stress responses in crop plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=ROS Regulation during abiotic stress responses in crop plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=You&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zallot R%2C Yazdani M%2C Goyer A%2C Ziemak MJ%2C Guan JC%2C McCarty DR%2C de Cr�cy%2DLagard V%2C Gerdes S%2C Garrett TJ%2C Benach J%2C Hunt JF%2C Shintani DK%2C Hanson AD %282014%29 Salvage of the thiamin pyri�m�idine moiety by plant TenA proteins lacking an active%2Dsite cysteine%2E Biochem J 463%3A 145%2D155&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zallot R, Yazdani M, Goyer A, Ziemak MJ, Guan JC, McCarty DR, de Cr�cy-Lagard V, Gerdes S, Garrett TJ, Benach J, Hunt JF, Shintani DK, Hanson AD (2014) Salvage of the thiamin pyri�m�idine moiety by plant TenA proteins lacking an active-site cysteine. Biochem J 463: 145-155

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zallot&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Salvage of the thiamin pyri�m�idine moiety by plant TenA proteins lacking an active-site cysteine&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Salvage of the thiamin pyri�m�idine moiety by plant TenA proteins lacking an active-site cysteine&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zallot&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zheng L%2C Huang F%2C Narsai R%2C Wu J%2C Giraud E%2C He F%2C Cheng L%2C Wang F%2C Wu P%2C Whelan J%2C Shou H %282009%29 Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings%2E Plant Physiol 151%3A 262%2D274&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, Shou H (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151: 262-274

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zheng&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zheng&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu YN%2C Shi DQ%2C Ruan MB%2C Zhang LL%2C Meng ZH%2C Liu J%2C Yang WC %282013%29 Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton %28Gossypium hirsutum L%2E%29%2E PLoS One 8%3A e80218&dopt=abstract

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http://scholar.google.com/scholar?as_q=Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


Does abiotic stress cause functional B vitamin deficiency? · ... D.R.M) and Food Science and Human...

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