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. 2017 Aug 8;8:1376. doi: 10.3389/fpls.2017.01376

Nitrate Uptake Affects Cell Wall Synthesis and Modeling

Simone Landi 1, Sergio Esposito 1,*
PMCID: PMC5550703  PMID: 28848580

Abstract

Nowadays, the relationship(s) about N assimilation and cell wall remodeling in plants remains generally unclear. Enzymes involved in cell wall synthesis/modification, and nitrogen transporters play a critical role in plant growth, differentiation, and response to external stimuli. In this review, a co-expression analysis of nitrate and ammonium transporters of Arabidopsis thaliana was performed in order to explore the functional connection of these proteins with cell-wall related enzymes. This approach highlighted a strict relationship between inorganic nitrogen transporters and cell wall formation, identifying a number of co-expressed remodeling enzymes. The enzymes involved in pectin and xyloglucan synthesis resulted particularly co-regulated together with nitrate carriers, suggesting a connection between nitrate assimilation and cell wall growth regulation. Major Facilitator Carriers, and one chloride channel, are similarly co-expressed with pectin lyase, pectinacetylesterase, and cellulose synthase. Contrarily, ammonium transporters show little or no connection with those genes involved in cell wall synthesis. Different aspects related to plant development, embryogenesis, and abiotic stress response will be discussed, given the importance in plant growth of cell wall synthesis and nitrate uptake. Intriguingly, the improvement of abiotic stress tolerance in crops concerns both these processes indicating the importance in sensing the environmental constraints and mediating a response. These evaluations could help to identify candidate genes for breeding purposes.

Keywords: abiotic stress, Arabidopsis, ammonium, tomato, xyloglucane synthesis, pectin synthesis, cellulose synthesis, nitrogen assimilation

Introduction

Cell wall development and remodeling are crucial processes for plants. The molecular and biochemical modifications of cell wall play critical roles in various aspects of plant physiology such as, differentiation, senescence, abscission, plant–pathogen interactions, abiotic stress response, plant growth, and others (Marowa et al., 2016). Cell wall is a necessary plant characteristic, mainly composed by polysaccharides, such as, cellulose and hemicellulose; pectins; lignin, and structural proteins (Guerriero et al., 2014, 2016). A major feature of the cell wall is its dynamic and active structure, remodeled during key stages of development, and in response to external stimuli. Therefore, during the plants life there is an incessant assembly, disassembly, and re-arrangement of the cell wall (Marowa et al., 2016). These processes are critical for plant development and acclimation, because the cell wall loosening is a direct cause of cells expansion and plant growth (Fukuda, 2014).

An interesting example is the cell wall remodeling during the stress response, by the activation of a wide range of enzymes involved in cell wall loosening (Tenhaken, 2015). This regulation represents a crucial point for tolerance to drought and salinity in crops (e.g., tomato; rice), when huge number of genes was differentially expressed upon stress (Iovieno et al., 2011; Landi et al., 2017b). Furthermore, cell wall is differently modified by biotic stress and pathogen attacks, revealing its functional plasticity (Bellincampi et al., 2014).

Among the mechanic modifications required for cell wall remodeling, the enzymes mainly involved include xiloglucan endotransglucosylase/hydrolase, expansine, enzymes involved in pectin modification (e.g., pectinesterase; pectin lyase), peroxidase (Tenhaken, 2015; Franciosini et al., 2017; Landi et al., 2017b). These enzymes are consistently regulated during nutrient deficiency (as nitrogen and/or sulfur deprivation), in order to allow the correct uptake of these elements (Fernandes et al., 2013). Particularly, N deficiency induces cell wall loosening: N is mainly assimilated in plants as nitrate (NO3-) by specific transporters (Fan et al., 2017). This family includes a number of carriers generally described as low or high affinity transporters, playing different roles depending on the soil availability of N. In addition, plants can assimilate N as ammonium (NH4+) by specific channels (Glass et al., 2002).

In the present study, an overview of the relationship between cell wall remodeling and nitrogen uptake will be provided. The co-expression analysis of Arabidopsis thaliana nitrate and ammonium transporters will be explored, in order to identify how cell wall enzymes relate to N assimilation, and clarify the concurrent processes involved in cell wall re-organization. A final survey with a perspective on the importance of N assimilation and cell wall modification upon abiotic stress will be given.

N uptake and cell wall remodeling: a co-expression analysis

The relationships between N accumulation and plant cell wall remodeling are argument of debate. The molecular cross-interactions between these processes are still unclear: therefore, nitrogen and ammonium transporters were identified in A. thaliana, and co-expression analysis was made using the ATTED-II software version 8.0 at http://atted.jp (Aoki et al., 2016).

In detail, six low affinity nitrate transporters (At1g12110, At1g69850, At1g32450, At1g27080, At1g69870, At4g21680), two “major facilitator super family” proteins (At1g52190, At3g16180), seven high affinity nitrate transporters (At1g08090, At1g08100, At5g60780, At5g60770, At1g12940, At3g45060, At5g14570), and six ammonium transporters (At4g13510, At1g64780, At1g64780, At4g28700, At3g24290, At2g38290) were selected at this purpose.

The chloride channel A (CLCA–At5g40890) was chosen based on its capability of 2 NO3-/1H+ exchange.

It should be noted that ammonium transporter 1.3 (AMT1.3–At1g64780); and 1.5 (AMT1.5–At3g24290) showed no co-expression in the database utilized, and thus these carriers were excluded in the present analysis.

Intriguingly, several cell wall related genes are co-expressed with nitrate and ammonium transporters (Table 1). Particularly, it is worth noting the presence of a number of enzymes involved in cell wall loosening: during nitrogen assimilation, a disassembly of the cell wall could be necessary for an enhanced N uptake, allowing a correct cell and plant growth. Furthermore, this behavior suggests that a right balance of cell wall loosening and thickening is desirable during plant growth, in order to correctly supply nutrients for biosynthesis of both primary and secondary cell walls. This balance could be enhanced by adequate nitrogen assimilation.

Table 1.

Co-expression analysis of Arabidopsis nitrogen and ammonium transporters, obtained using the ATTED-II database.

A. THALIANA LOW AFFINITY NITRATE TRANSPORTER A. THALIANA AMMONIUM TRANSPORTER
At1g12110 NT 1.1. At1g69850 NT 1.2. At1G32450 NT 1.5 At1G27080 NT 1.6 At1g69870 NT 1.7. At4g21680 NT 1.8. At4g13510 AMT 1.1 At1g64780 AMT 1.2 At4g28700 AMT 1.4 At2g38290 AMT 2
Guard cells–lateral roots Roots hairs and epidermids Roots pericycle cells Vascular tissue of funiculus and silique Phloem Xylem Plasma membrane Endodermal and cortical cells of root Plasma membrane–leaf, flower, pollen Plasma membrane and cytoplasm
Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR
PMA2 4 FMO 4.6 HAD 1 CESA10 3.2 Major facilitator 1.4 TH8 3 Lipase 5 CLC-B 3.5 At5g19270 3 ERD6 5.6
NIR1 7.1 Hydrolase 8.4 PHO1 2.8 DUF821 6.9 UGT84A3 1.7 LTP 5.5 GSR 1 5.7 Cysteineases 4.4 Galactose oxidase 5.2 SERK3 6
NR1 7.9 Transcription 8.4 At2g28780 3.9 TLP5 7 Major facilitator 2 Rap2.6L 5.6 Kinase 9.4 Transporter 5.7 RmlC-like cupins 8.9 UGT71C5 9.4
REF1 13.2 CNGC5 17 UMAMIT18 4.9 RGP4 7.3 CAX7 3 UGT76E12 13.4 LHT1 9.9 At2g15020 11.5 At1g15830 9.8 RLK7 11.2
GSR2 16.3 TBL40 18.9 MYB59 5.3 ASD2 7.8 GPT2 4.2 BGLU11 13.4 PP 2C 9.9 cPT4 16.3 galactokinase 10.6 PGP21 11.4
UGT72E1 18.4 ACR3 20.4 DUF599 5.5 BAN 8.8 YSL1 5.5 XTH11 16.7 AMT2 14.1 At3g56290 18.8 inhibitor 10.9 AMT1;1 14.1
SULTR1;2 19.6 Plant calmodulin 22.2 Galactose mutarotase 6.3 MYB5 9.2 Protease 6.3 Nitrate transporter 2.6 19.4 HIR2 17.8 NAS1 19.4 Ubiquitin-like 16 EXO70B2 14.6
PSY1R 21.4 XIP1 22.3 UMAMIT29 6.7 UGT73C2 10.4 Transferase 6.5 Related to AP2 6 24.4 PEN3 18.5 MYC4 19.6 UPF0497 17 kinase 16.9
FMO GS-OX5 29.7 PSY1R 31 DUF716 8.1 ligase 12 MATE efflux 6.7 SRG2 24.4 PLAC8 18.7 At5g19970 21.2 AGL57 17.5 IQM1 19.8
GTR2 37.1 XLG1 35.6 MYB48 8.7 CYP709B1 12 SPSA1 9.2 GLYI7 27.6 RLK 18.9 Transferase 22.7 At1g15840 20.2 Transmembranes 14C 20.7
TIP2;2 39.4 ADR1-L1 38.2 HMA4 9.2 Major facilitator 12.7 PES1 10.8 DIN11 29.6 PMR2 22.2 myb 25.3 At2g22060 23 transferase 20.8
G6PD2 40.1 Galactose oxidase 49.1 Oxidoreductase 10.6 Major facilitator 12.7 JR2 12 DNA-binding 30.2 BIR1 23.1 XTR8 26.5 Glycine-rich 23.4 BIK1 21
CYP71B7 41.4 TET5 52.8 Major facilitator 10.9 RmlC-like cupins 16.3 UGT71B1 12.4 ORS1 33.7 PMT5 26.9 Transferase 29.5 Transferase 24.4 Isomerase 22.4
Chaperonin 46 XTH27 54.4 Endopeptidase 11.5 Transferase 18 MT2A 13.9 GSTU4 34.2 DUR3 29.9 FADA 29.9 Transposable 25.1 Hydrolase 23.4
Transcription 48.1 PHX21 57.5 At2g21560 11.8 TT10 20.9 LOX2 14 SRG1 36.1 Major facilitator 32.4 CAT2 30 CSLD6 26.1 CRK29 23.5
CA4 52 UGE1 57.8 UMAMIT17 12.2 MBOAT 21.9 Tetratricopeptide 14.5 Decarboxylase 46.9 Chitinase 33 GBSS1 30.8 IDH-III 26.5 SUC1 24.2
UPM1 55 STP4 58.7 VIT 12.4 Hydrolase 23.8 transferase 17.6 2OG 47 WR3 33.3 Glutaredoxin 34.6 CHX25 27.7 BIR1 24.6
NR2 56.4 Leucine-rich repeat 58.8 DUF599 13 OPT5 24.7 COR15A 21.2 AGP10 47 MCP1c 36.2 CAD4 35.9 GRP17 28.6 CRK28 25.6
Zinc finger 58.6 SET7/9 59 UMAMIT31 13.1 DUF579 25.7 SWEET4 21.5 NAC019 49.8 ERD6 40.1 dirigent-like 36.6 COPT3 31 Zinc finger 26.4
AAP5 58.7 Protein kinase 59.3 SLAH1 13.4 MES19 27.8 UGT76E11 22.6 Major facilitator 51.2 SOBIR1 40.7 ACN1 37.5 ENODL22 32.5 XBAT34 27.5
KT1 59.1 At3g52240 62.6 UMAMIT30 13.9 UMAMIT15 28.8 transporter 23.8 XTR6 51.9 ACA11 43.1 PME1 40.7 TIR-NBS-LRR 33.3 CNGC10 30.9
Oxidoreductase 67.5 Related to AP2 2 69.5 Major facilitator 14.5 Pectinacetylesterase 30 NAT2 28.4 NAC3 54.2 Protease 44.7 PRH43 41 At3g44140 34.5 At2g18690 31.1
TBL27 69.2 NPC1 70.3 AAP2 14.9 MBOAT 30.3 GDSL Hydolase 29.9 Rossmann-fold 54.5 EXO70B2 45.3 SPS2 41.8 Glycine-rich 35.1 FAD binding Berberine 32.5
LEA 71.6 PMIT1 70.4 Glycine-rich 14.9 SHP2 30.9 MATE efflux 30.4 AKR4C8 55.3 ALA1 46.6 NCS1 42 UGT84B2 36.9 PLAC8 34.6
Transporter 72.8 Duplicated homeodomain 72.4 Transporter 15 Rossmann-fold 31.8 ZHD10 33.3 ILR1 57.9 STP4 47.2 At5g43150 42.1 At2g18115 37.4 WCOR413 37.5
UGT84A4 75.9 DUF946 73.2 At4g34600 15 Inhibitor 32.8 PSK5 35.4 Transferase 66.5 Kinase 52.6 COPT2 42.6 DUF220 40 Kinase 38.6
Transferase 76.2 Fragile-X-F-associated 77.1 DNA-binding 15.2 IPT6 34.2 Major facilitator 35.8 CAD1 67.4 IQM1 53.1 PSY1R 45.2 Transposable 41.4 SYR1 39.1
EFE 82.8 At2g17710 77.5 UMAMIT28 15.3 MES4 34.4 CCT motif 36.4 Oxidoreductase 71.7 CRK19 53.2 Major facilitator 47.2 Plant self-incompatibility 41.4 MATE efflux 40.1
HAD 85.5 SEC14 cytosolic factor 80.5 UMAMIT20 16 TT12 36.5 RLP33 37.6 BT4 72.8 SERK3 53.6 SIGE 48 Major facilitator 45.2 At4g25030 40.1
CSY4 88.4 GASA1 86.4 UMAMIT11 17.8 Peroxidase 37.1 NAC019 38.8 PRX52 73.5 Kinase 53.8 ADT6 48.1 VIT 45.5 PLAC8 42.4
MAJOR FACILITATOR SUPER FAMILY A. THALIANA HIGH AFFINITY NITRATE TRANSPORTER Chloride Channel
At1g52190 NT 1.11 At3g16180 NT 1.12 At1g08090 NT 2.1. At1g08100 NT 2.2. At5g60780 NT 2.3 At5g60770 NT 2.4 At1g12940 NT 2.5 At3g45060 NT 2.6 At5g14570 NT 2.7 At5g40890 CLCA
Plasma membrane—leaf phloem Plasma membrane—leaf phloem Plasma membrane—root, shoot Plasma membrane plasma membrane–shoot apex, vascular leaf Plasma membrane Guard cells–Inflorescence–stem Chloroplast–flower, guard cells, root Tonoplast–reproductive organs and seeds Cellular and vacuolar membrane
Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR Co-expressed genes MR
Pectin lyase-like 1.7 TUB5 4.2 PP2C 1 Nitrate transporter 2.4 1.4 At5g38320 2 PP2C 6 GLN1;4 1 Nitrate transporter 2.3 3.5 GDSL-like Lipase 6.6 VAC-INV 1.4
IAA7 2.2 WLIM2a 9.2 Oxygenase 3.2 PP2C 2.5 Nitrate transporter 2.3 3.5 Hydroxylase 14 Thioredoxin 15.2 DNA-binding 6.9 AER 8.7 At1g49500 1.4
Domain 3.3 TUB1 9.6 HPP 6 MBD3 2.5 Inhibitor 3.5 Cysteine/ Histidine-rich 22.4 YSL7 20.9 Inhibitor 15.3 At5g64230 11.6 Hydrolase 6.3
Glycosylase 3.5 DUF1645 9.8 RWP-RK 6.3 Oxygenase 3.3 PRB1 4.2 GNS1/SUR4 membrane 26.5 FRK1 26 Nitrate transporter 1.8 19.4 Heavy metal detox 13.9 TIP2 6.7
Pectin lyase-like 4.2 DRT100 10.7 TIR-NBS-LRR 6.9 NRT2;1AT 7.1 LMI1 39.1 CSLB02 28.2 CAT1 26.5 WRKY28 24.9 G3Pp4 15.2 PIP1A 8.5
LUP1 4.4 PGP19 12.7 GSTF14 12.4 HPP 13.2 ASML2 41.7 CYP702A2 36.9 Cysteine/Histidine-rich 27.8 DUF642 37.4 RCC1 15.5 PIRL4 8.5
PKS2 4.6 Transferase 15.2 WR3 13.8 RWP-RK 21.9 SUC6 44.5 MBOAT 38.5 CAT5 40.6 LTP 38.2 Transporter 18.4 Beta-xylosidase 1 9.4
PIN7 4.9 ERD3 15.4 NAS2 18 TIR-NBS-LRR 54.7 Transcription 52.6 Mannose-binding lectin 40.6 Transporter 47.8 SHB1 53 GolS3 21.6 HAD 10
P1R1 5.7 Transferase 15.9 PP2-A3 19.3 Transferase 60.2 NUB 70.6 CYP96A14P 45.1 NAC048 53.8 MLO12 57.5 Nitrate transporter 1.7 23.8 SPF1 10
BEE2 6 DNA-binding 17.9 At5g10210 20.4 LEA3 62.7 Peroxidase 80.9 Terpenoid synthases 49.6 ZIP5 55.6 SLAH2 65.7 At1g68500 24.2 PATELLIN1 12.1
DGR2 6.9 Glycosylase 18.8 Kinase 28.6 Transposable 72.2 Transferase 86.5 DC1 55.7 CHX16 59.7 CAT1 70.7 At3g19920 31.8 phosphoesterase 14.4
TCP15 7.3 Pectin lyase-like 18.9 TIR-NBS-LRR 34.6 GSTU21 100.5 DNA-binding 102.1 WSD1-like 57 Inhibitor 63.9 Zinc finger 73 DNA bromodomain 41.6 beta glucosidase 16 15
At1g67050 7.6 Kinase 20.7 Pectin lyase-like 37.1 Glutamate receptor 101.5 PP2C 104.9 TLC 67.7 RLP21 78.2 WRKY8 76.8 Glycosyl hydrolase 42.7 TauE/SafE 15.4
DWF3 7.8 LYK3 21.9 Glutamate receptor 37.2 At1g49260 103.4 LEA 120.1 Terpenoid synthases 69.5 OPT1 78.4 YSL7 77.6 chaperonin 44.9 beta galactosidase 17.2
DUF642 9.5 TRM2 22.2 Major facilitator 46.9 DNA-binding 105.7 RPP27 123.9 DNA-binding 90.7 Thioredoxin 79 Kinase 79.3 UDP-Glycosyltransf 46.6 TMP-A 18
GASA6 9.9 Major facilitator 24.2 Kinase 48.4 DNA-binding 116.8 UMAMIT32 133.1 Transporter 94.5 DNA-binding 79.3 Cysteine/ Histidine domain 81.8 UGT76E11 54.4 Phosphorylase 21
PRA1.F1 11.5 Pectinacetylesterase 24.3 Protease 48.8 Cysteine/ Histidine-rich 118.5 HDG4 151.6 Cysteine/ Histidine-rich 101.2 RWP-RK 80.7 transporter 94.4 GIA1 60.7 PIP1D 22.2
WAV5 12 RPT3 25.1 RING/U-box 49.5 At4g16090 127.1 F-box 154.6 Oxidoreductase 105.7 Kinase 87.7 Major facilitator 94.9 CYP72A15 64.7 Major Facilitator 23.4
TIP2;1 12.2 Gibberellin-regulated 26.8 Kinase 53.5 Transposable 128.1 Transposable 173.5 RWP-RK 119.8 CRK24 90.3 WR3 96.6 LKP2 65.6 Pectin-lyase like 25.4
Phosphoesterase 12.4 PLA2-ALPHA 27.5 PGM 55.5 At2g18610 129.1 F-box 188.1 Cysteine/ Histidine-rich 125.7 MCP1c 92.8 SAUR-like auxin-responsive 96.8 LEA 68.3 PIP2A 25.4
Pectin lyase-like 14 At3g52500 27.8 Peroxidase 57.8 At3g50250 130.2 At5g48200 200.8 At1g07680 136 ACR6 96.3 2OG 97.6 TLC 69.2 Major Facilitator 26.3
EXPA11 14.5 Homeodomain-like 29.1 Ca-dep lipid-binding 60.3 Kinase 132.5 Transposable 205 Peroxidase 136.2 Bifunctional inhibitor 104.1 Kinase 99.8 DNase 69.3 CSLA3 26.5
PIN4 14.6 FRUCT5 29.6 TAC1 60.7 PUP15 139.5 At5g28800 211.6 Cysteine/ Histidine-rich 138.1 At1g51920 123.5 Transposable 111.1 COR15B 71.5 ZYK4 26.8
Phosphodiesterases 14.7 GRH1 31.4 Kinase 60.8 At1g53640 141 At4g16090 211.8 Transposable 140.8 PTR3 128.2 MYB2 124.1 SOM 76.7 ATRR4 27
DUF617 16.4 PME3 33.9 TIR-NBS 61.5 Kinase 157 At4g11930 223.8 PLAC8 144.3 zinc finger 132.4 SS3 124.8 RLP33 77.5 Pectin-lyase like 29.8
EXPA8 16.9 TUB6 35.1 SAUR-like 64.5 C2 161.5 Transferase 235.6 Cysteine/ Histidine-rich 145 lectin receptor kinase 132.8 Nitrate transporter 2.1 125.4 CHY2 81.2 PSY1-R 29.9
Pectin lyase-like 17.7 TET7 36.3 G6PD3 71.3 At3g44140 173.9 Galactose oxidase 237.3 PEN2 146.2 Lipase class 3 135.7 Kinase 133.7 Na/Ca exchanger 84.3 TMK-1 30.2
TCP11 19.8 TBR 37.4 GSTU21 76.8 LEA 180.1 RING/U-box 244.9 Cysteine/ Histidine-rich 146.2 DUF1218 138 Kinase 136.2 RD29A 87.5 TIP1:2 30.7
Glycosylase 20.4 Kinase 39.5 Kinase 77.1 Kinase 183.1 Transposable 247 CSLB01 146.6 RLK6 139.8 ELI3-2 139.7 At1g21670 90.1 At3g27390 33
EXP3 20.8 XTH4 42.7 Cysteine/ Histidine-rich 79.5 Pectin lyase-like 256.4 Separase 249.5 PRA1.G1 149.8 SHB1 139.9 Plant invertase 202.1 Glycosyl hydrolase 108.5 SnRK3.17 33
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The co-expression degree was estimated as Mutual Rank (MR), as described by Aoki et al. (2016), and shown on the right side of each column. Cell wall related genes (yellow highlighting genes) were identified by Gene Onthology categories.

The identification of the main interesting cell wall related genes is as follow: At3g52500 (Eukaryotic aspartyl protease); Bifunctional inhibitor (Bifunctional inhibitor/lipid-transfer protein/Seed storage 25 albumin protein); CESA and CSLB (Cellulose synthase); CSY (Citrate synthase); DGR2 (Protein with unknown function); DUF (Protein with unknown function); Dirigent (Disease resistance-responsive dirigent like protein); Endopeptidase (Substilin-like serine endopeptidase family protein); EXPA (Expansin); EXP3 (Barwin like endoglucanase protein); FRUCT5 (Beta-fructofuranosidase 5); GASA (GAST1 protein homolog); GDSL hydrolase (GDSL-like Lipase/Acryhydrolase protein); GSR (Glutamine syntethase); HAD (HAD superfamily, subfamily IIIB acid phosphatase); Plant invertase (Plant invertase/pectin methylesterase inhibitor superfamily); PME (Pectin methylesterase 3); PRX (Peroxidase); SS3 (Strictosidine synthase 3); TBL (Protein with unknown function); TIP2:1 (Tonoplast intrinsic protein); TUB5 (tubulin beta-5 chain); UGE (UDP-D-glucose/UDP-D-galactose 4-epimerase 1); XTR (Xyloglucan endo-transglycosylase); XTH (xyloglucan-endotransglucosylases/hydrolases).

Consistent with these considerations, Fernandes et al. (2016) showed a diversified molecular expression of the cell wall loosening related genes in Vitis viniferae callus subjected to nitrogen, sulfur, and phosphorus deficiency, highlighting that N affects the cell wall responses more severely than other nutrients.

As shown in Table 1, low affinity and high affinity nitrate transporters showed similar number and type of cell wall related co-expressed genes. Otherwise, ammonium transporters showed a lower co-expression with cell wall related genes; this would probably suggest minor, or absent relationship(s) with cell wall remodeling.

Examples of cell wall remodeling genes which appear related to nitrogen transport are pectinase, involved in pectin degradation, such pectin lyase (At4g23820, At3g07010, At3g16850, At5g48900, At5g14650, At3g57790, At3g16850), pectinacetylesterase (At1g09550, At5g23870), or pectin methylesterase (At3g14310). Particularly, the cleavage of homogalacturonans by pectinesterases produces substrates for polygalacturonase and pectin lyase, acting in the cleavage of the polygalacturonic acid (Sun and Nocker, 2010).

These genes are important members of fruits' maturation network (Marín-Rodríguez et al., 2002), and previous studies described their involvement in the abiotic stress response (Hong et al., 2010; Tenhaken, 2015; Landi et al., 2017b). It has been proposed that pectins are able to form gel structures that increase cell wall consistency (Fernandes et al., 2016).

The activation of pectinase(s) together with nitrogen transporters could induce the relaxation of the cell wall.

Other important actions associated with nitrogen uptake are the modification of xyloglucans. A number of enzymes involved in this process were co-expressed with nitrate transporter such xyloglucan-endotransglucosylases/hydrolases (XTH—e.g., At3g44990, At3g48580, At2g06850), xyloglucan-endo/transglycosilase (XTR—e.g., At4g25810), and expansins (e.g., At1g20190–At2g40610). Xyloglucans are the major hemicellulosic polymers of dicot plants, playing a critical role in cellulose fibrils connection. Modification in their content is an important process regulating several physiological plant responses by the cell wall remodeling (Tenhaken, 2015; Marowa et al., 2016). It was proposed that xyloglucan regulation by expansins could improve the efficiency of nutrient uptake. In fact, several types of expansins respond to different nutrient deficiencies including nitrogen, phosphorus, potassium, and iron ones (Li et al., 2014).

Furthermore, expansins have been proved to play a pivotal role in several aspects such fruit ripening and softening, abiotic stress tolerance, and crops yield (Zhou et al., 2014; Minoia et al., 2015; Marowa et al., 2016).

Interestingly, the major facilitator superfamily genes At1g52190–AtNT 1.11 and At3g16180–AtNT1.12 are consistently co-expressed together with several cell wall relaxation genes; it must be underlined that these transporters play an important role in plant physiology translocating nitrate from phloem to xylem.

Particularly, their action appears critical for high-nitrate-enhanced shoot growth, and for nitrate translocation from old to young leaves. These processes represent key points affecting biomass production, and crop yield (Hsu and Tsay, 2013).

Finally, nitrate transporter and cell wall related processes are connected also during embryogenesis. The AtNRT1.6 is expressed in reproductive tissues, namely vascular tissue of the silique and funiculus. This transporter plays a critical role during early embryogenesis phase (Almagro et al., 2008): interestingly, this gene was co-expressed with cellulose synthase A (CESA–At2g25540). Previous studies reported that several members of this family are necessary for a correct embryogenesis (Beeckman et al., 2002; Goubet et al., 2003). This evidence corroborated the idea of a strict connection between nitrogen uptake and cell wall regulation in various aspects of plant development and morphogenesis.

The relationship between nitrogen transporter and cell wall upon abiotic stress

It is worth to point out that both nitrate transporters and cell wall remodeling enzymes play crucial roles in response to various abiotic stresses (Tenhaken, 2015; Fernandes et al., 2016; Fan et al., 2017; Landi et al., 2017b).

Among nitrate transporters, AtNRT1.1 (At1g12110) was identified as a salt and drought stress responsive gene (Guo et al., 2003; Álvarez-Aragón and Rodríguez-Navarro, 2017). This gene is expressed in guard cells and plays an important role in stomata opening: AtNRT1.1. mutants showed an enhanced drought tolerance (Guo et al., 2003).

Further, AtNRT.1.1 plays a major role in Na+ and Cl− assimilation in both normal and high salinity conditions, suggesting its role in salt stress tolerance (Álvarez-Aragón and Rodríguez-Navarro, 2017). Interestingly, co-expression analysis showed this gene less co-expressed with cell wall related genes (Table 1): this confirms that cell wall remodeling genes were diversely down-regulated during abiotic stress in order to limit the damage (Leucci et al., 2008). Intriguingly, AtNRT1.1. showed a number of stress-related coexpressed genes such as, tonoplast intrinsic protein (TIPs–At4g17340), glucose-6P dehydrogenase (G6PDH–At5g13110), heat shock proteins (HSP–At5g02480), late embryogenesis proteins (LEA–At3g52470; Boursiac et al., 2005; Ma et al., 2006; Basile et al., 2011; Esposito, 2016; Landi et al., 2017a), thus highlighting its role in abiotic stress response (Table 1).

Another interesting nitrate transporter involved in abiotic stress response is AtNRT1.8 (At4g21680): cadmium (Cd++) stress strongly stimulated the accumulation of this transporter in roots, and A. thaliana plants with mutated AtNRT1.8 showed increased sensibility to Cd++ stress (Gojon and Gaymard, 2010). Intriguingly, as showed in Table 1, AtNRT1.8 is co-expressed with a number of cell wall related genes, namely XTH11 (xyloglucan-endotransglucosylases/hydrolases), XTR6 (xyloglucan-endo/transglycosilase), and PRX52 (peroxidase superfamily). Particularly, peroxidase activity was assisted by a number of antioxidant enzymes such as, glutathione S-transferase (GSTU4), NAD(P)-linked oxidoreductase (AKR4C8), and others (Table 1). This could be necessary to regulate the increased of reactive oxygen species (e.g., H2O2), enhancing the mechanical stability of the cell wall, and thus stress tolerance (Tenhaken, 2015).

Further, CLCA (At5g40890) is a chloride channel that plays a role as NO3-/H+ exchanger, useful to accumulate nitrate in vacuoles (De Angeli et al., 2006). Recently, this transporter was reported as related to PP2A-C5 (At1g69960) during salt stress response (Hu et al., 2017); the co-expression analysis showed a relationship with cell wall related proteins such as, pectin lyase (At3g57790 and At3g16850); cellulose synthase C; and with aquaporines such TIPs (tonoplast intrinsic proteins) and PIPs (Plasma membrane intrinsic proteins). The co-expression of TIP2 (At3g26520) and TIP2.1 (At3g16240) confirms the critical role of CLCA in nitrate translocation into the vacuoles as well. Interestingly, NTR1.1 is co-expressed with tonoplast intrinsic protein TIP2.2 (At4g17340). Particularly, nitrate allocation from/to vacuoles suggested a central role during plant adaption in N-rich and N-deficient environments (Fan et al., 2017). Recent evidence indicated the role of phosphatidylinositol-3,5-bisphosphate as signal for nitrate translocation in vacuoles by the activation of CLCA (Carpaneto et al., 2017).

Further, the regulation of the nitrate allocation into the vacuoles was assisted by peptide transporters (PTRs), such as, AtPTR4 (At2g02020) and AtPTR6 (At1g62200); these proteins showed vacuole specific localization, thus playing a role in nitrate storage in the plant cell (Weichert et al., 2012). Fan et al. (2017) reported that NRT2.1 plays an important role in resistance to drought. This action was reported in different species such as, Arabidopsis and Brassica, together with NRT1.1 and NRT1.5 (Goel and Singh, 2015; Fan et al., 2017). Other authors reported that NRT2.1 regulated root hydraulic conductivity, by altering NO3- accumulation (Li et al., 2016). Furthermore, this nitrate transporter positively regulates the translational levels of PIPs; the bioinformatic analysis highlights the co-expression of this transporter with cell wall related genes, such pectin lyase and peroxidase; and with abiotic stress related genes such protein phosphatase 2C (PP2C), glutathione S-transferase (GST), G6PDH, and others, thus confirming that nitrogen transporters, cell wall remodeling enzymes, and others genes together contributes for abiotic stress tolerance.

Transcriptomic modification in adverse environment: nitrate and cell wall candidates genes for tolerance in crops

Nowadays, next generation sequencing (NGS) provides for new insight into crops genetic breeding, generating huge amount of data, mapping across crops population, and discovering useful genes, QTL and genomic traits (Cobb et al., 2013).

The improvement of tolerance in crops vs. abiotic stress remains today an important focus for plant biology researchers because this reduces plant growth, development, and productivity (Reynolds and Tuberosa, 2008; Cardi et al., 2015; Ruggiero et al., 2017). This promising strategy can be prosecuted by applying modern molecular and -omics techniques, together with the study and the analysis of traditional landraces (Van Oosten et al., 2016; Landi et al., 2017a,b). In the last years, many researchers investigated this topic using NGS; in tomato (Solanum lycopersicum), 966 differential expressed genes (DEGs) have been identified upon drought; among these, at least 50 genes involved in cell wall remodeling and nitrate transport were identified. Particularly, 20 clusters of genes were grouped, and their transcripts show similar expression trends (Iovieno et al., 2011).

Some clusters showed interesting correlations: in cluster 4, expansin (Solyc06g049050), nitrate transporter (Solyc12g006050), cellulose synthase (Solyc04g071650), and XTH (Solyc02g091920); in cluster 5, cellulose synthase (Solyc04g077470), expansin (Solyc02g088100), nitrate transporter (Solyc03g113250), and XTH (Solyc07g052980).

Similarly to other abiotic stress, nutrient deprivation negatively influences crops yield. Nitrogen deficiency is a critical cause of yield loss, but N fertilizer consumption has become one of the major costs of crop production (Zhao et al., 2015).

A huge transcriptomic modification in durum wheat (Triticum turgidum) upon nitrogen starvation highlighted 4,626 DEGs in different organs such as, roots, leaves, stems, and spikes (Curci et al., 2017). An interesting enrichment of GO categories related to “Cell Wall Biogenesis” and “Cellulose metabolism” in leaves was reported, highlighting the relationship between nitrogen nutrition and regulation of the integrity of cell wall. Also, a number of up-regulated high affinity nitrate transporters in root and flag leaf (e.g., NT2.3 and NT2.5) were found, while numerous cell wall related genes showing a transcriptional regulation induced by nitrogen starvation. Examples of these are pectin lyase, expansin, and wall associated kinase (WAK). Particularly, WAKs play critical roles in root growth under N limitation (Kiba and Krapp, 2016). Intriguingly, the correlation among WAKs and nitrogen deficiency was also observed in two lines of Tibetan barley (Hordeum vulgare) expressing nitrogen transporter with genomic variants (Quan et al., 2016).

Moreover, nitrogen starvation was studied in rice (Oryza sativa; Yang et al., 2015). This stress induced the modification in the expression of 1,158 genes in leaves, and 492 in roots. Part of these were identified as cell wall related genes: in roots it has been reported the expression of few genes involved in cell wall degradation, such fasciclin-like arabinogalactan protein (Os10t0524300), and sulfated surface glycoprotein (Os10t0524300). On the contrary, in leaves a higher number of DEGs related to various aspects of cell wall regulation was reported, such fasciclin-like arabinogalactan protein (Os01t0668100), beta-galactosidase (Os06t0573600), UDP-glucuronic acid decarboxylase (Os03t0278000), and expansin (Os10t0555900, Os10t0556100).

Recently, Zhao et al. (2015) reported interesting results about the response of cucumber (Cucumis sativus) at early nitrogen shortage. Among the top enriched GO categories, the presence of genes encoding for proteins and enzymes involved in xyloglucan transferase activity were reported, underlining their role(s) in cell wall synthesis and remodeling. Further, a number of genes involved in cell wall loosening, cell expansion or cell wall component synthesis, including pectin lyases (Csa1G049960), XTH (Csa1G188680), pectinesterases (Csa7G447990; Csa7G343850), and expansin (Csa5G517210) were grouped in different expression clusters, and regulated during the early stage of N deficiency response. Thus, pectins breakdown under N deficiency would provide substrates to other biological processes, compensating for the depressed photosynthetic carbon assimilation. In addition, a connection between cell wall degradation and ascorbic acid metabolism can be hypothesized, in order to provide an improvement of fruit quality upon N deficiency (Zhao et al., 2015).

Interestingly, cell wall related and nitrate transporter genes interact also during heavy metal stress such as, aluminum excess (Li et al., 2017). It has been reported a critical role for the STOP1/ART1, a zinc finger transcription factor, which induced the expression of a number of genes related to the aluminum toxicity tolerance in crops (Yamaji et al., 2009).

The effectors of STOP1/ART1 suggest a correlation in tea plants (Camelia sinensis) among cell wall related enzymes (e.g., expansine and polygalacturonase); membrane proteins (e.g., magnesium transporter, UDP-glucosyl transferase, and potassium transporter); detoxification proteins (e.g., Heat shock protein 20) and nitrate transporters. Therefore, a major role in the aluminum allocation for tolerance, or accumulation, has been proposed for this protein network (Li et al., 2017). A schematic summary, describing the key events during drought, salt and N starvation responses, and their relationships between nitrogen uptake and cell wall remodeling, is proposed in Figure 1.

Figure 1.

Figure 1

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Main effects induced by drought, salinity and nitrogen starvation on nitrogen assimilation and cell wall remodeling in plants.

Conclusions

This review provided for an updated survey between the correlation of nitrogen assimilation and cell wall related genes. These genes contribute together in several aspects of plant growth, physiology, and response to external stimuli. Evidences here described strongly support the notion of an involvement of NT and cell wall remodeling genes (e.g., pectin lyase, XTH, expansin) as a part of complex machinery involved in abiotic stress response in crops.

Further, cell wall related genes play a role in N starvation inducing cell wall relaxation and helping N assimilation. Therefore, these gene families could represent promising traits for genetic improvement in abiotic stress tolerance.

Author contributions

SL and SE conceived the idea and wrote the manuscript.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

SE acknowledges funding by “Benessere dalle BioTecnologie: Nuovi Processi e Prodotti per la Nutraceutica, la Cosmeceutica e la Nutrizione umana (BenTeN)” by Regione Campania – D.R. n° 199 26Oct2011; and 254/2011.

References

  1. Almagro A., Lin S. H., Tsay Y. F. (2008). Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell. 20, 3289–3299. 10.1105/tpc.107.056788 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aoki Y., Okamura Y., Tadaka S., Kinoshita K., Obayashi T. (2016). ATTED-II in 2016: A plant co expression database towards lineage-specific co-expression. Plant Cell Physiol. 57:e5 10.1093/pcp/pcv165 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Álvarez-Aragón R., Rodríguez-Navarro A. (2017). Nitrate-dependent shoot sodium accumulation and osmotic functions of sodium in Arabidopsis under saline conditions. Plant J. 91, 208–219. 10.1111/tpj.13556 [DOI] [PubMed] [Google Scholar]
  4. Basile A., Sorbo S., Golia B., Montanari S., Castaldo-Cobianchi R., Esposito S. (2011). Antioxidant activity in extracts of Leptodictyum riparium (Bryophyta), stressed by heavy metal, heat shock, and salinity. Plant Biosyst. 145, 77–80. 10.1080/11263504.2010.509935 [DOI] [Google Scholar]
  5. Beeckman T., Przemeck G. K., Stamatiou G., Lau R., Terryn N., De Rycke R., et al. (2002). Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiol. 130, 1883–1893. 10.1104/pp.102.010603 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bellincampi D., Cervone F., Lionetti V. (2014). Plant cell wall dynamics and wall-related susceptibility in plant-pathogen interactions. Front. Plant Sci. 5:228. 10.3389/fpls.2014.00228 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boursiac Y., Chen S., Luu D. T., Sorieul M., van den Dries N., Maurel C. (2005). Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol. 139, 790–805. 10.1104/pp.105.065029 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cardi M., Castiglia D., Ferrara M., Guerriero G., Chiurazzi M., Esposito S. (2015). The effects of salt stress cause a diversion of basal metabolism in barley roots: possible different roles for glucose-6-phosphate dehydrogenase isoforms. Plant Physiol. Biochem. 86, 44–54. 10.1016/j.plaphy.2014.11.001 [DOI] [PubMed] [Google Scholar]
  9. Carpaneto A., Boccaccio A., Lagostena L., Di Zanni E., Scholz-Starke J. (2017). The signaling lipid phosphatidylinositol-3,5-bisphosphate targets plant CLC-a anion/H+ activity. EMBO Rep. 18, 1110–1107. 10.15252/embr.201643814 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cobb J. N., Declerck G., Greenberg A., Clark R., McCouch S. (2013). Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype-phenotype relationships and its relevance to crop improvement. Theor. Appl. Genet. 126, 867–887. 10.1007/s00122-013-2066-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Curci P. L., Aiese Cigliano R., Zuluaga D. L., Janni M., Sanseverino W., Sonnante G. (2017). Transcriptomic response of durum wheat to nitrogen starvation. Sci Rep. 7:1176. 10.1038/s41598-017-01377-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. De Angeli A., Monachello D., Ephritikhine G., Frachisse J. M., Thomine S., Gambale F., et al. (2006). The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939–942. 10.1038/nature05013 [DOI] [PubMed] [Google Scholar]
  13. Esposito S. (2016). Nitrogen assimilation, abiotic stress and glucose-6-phosphate dehydrogenase: the full circle of reductants. Plants 5:24. 10.3390/plants5020024 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fan X., Naz M., Fan X., Xuan W., Miller A. J., Xu G. (2017). Plant nitrate transporters: from gene function to application. J. Exp. Bot. 68, 2463–2475. 10.1093/jxb/erx011 [DOI] [PubMed] [Google Scholar]
  15. Fernandes J. C., García-Angulo P., Goulao L. F., Acebes J. L., Amâncio S. (2013). Mineral stress_ affects the cell wall composition of grapevine (Vitis vinifera L.) callus. Plant Sci. 205–206, 111–120. 10.1016/j.plantsci.2013.01.013 [DOI] [PubMed] [Google Scholar]
  16. Fernandes J. C., Goulao L. F., Amâncio S. (2016). Regulation of cell wall remodeling in grapevine (Vitis vinifera L.) callus under individual mineral stress deficiency. J. Plant Physiol. 190, 95–105. 10.1016/j.jplph.2015.10.007 [DOI] [PubMed] [Google Scholar]
  17. Franciosini A., Rymen B., Shibata M., Favero D. S., Sugimoto K. (2017). Molecular networks orchestrating plant cell growth. Curr. Opin. Plant Biol. 35, 98–104. 10.1016/j.pbi.2016.11.010 [DOI] [PubMed] [Google Scholar]
  18. Fukuda H. (2014). Plant Cell Wall Patterning and Cell Shape. Hoboken, NJ: Wiley. [Google Scholar]
  19. Glass A. D., Britto D. T., Kaiser B. N., Kinghorn J. R., Kronzucker H. J., Kumar A., et al. (2002). The regulation of nitrate and ammonium transport systems in plants. J. Exp. Bot. 53, 855–864. 10.1093/jexbot/53.370.855 [DOI] [PubMed] [Google Scholar]
  20. Goel P., Singh A. K. (2015). Abiotic stresses downregulate key genes involved in nitrogen uptake and assimilation in Brassica juncea L. PLoS ONE 10:e0143645. 10.1371/journal.pone.0143645 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gojon A., Gaymard F. (2010). Keeping nitrate in the roots: an unexpected requirement for cadmium tolerance in plants. J. Mol. Cell Biol. 2, 299–301. 10.1093/jmcb/mjq019 [DOI] [PubMed] [Google Scholar]
  22. Goubet F., Misrahi A., Park S. K., Zhang Z., Twell D., Dupree P. (2003). AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol. 131, 547–557. 10.1104/pp.014555 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Guerriero G., Hausman J. F., Strauss J., Ertan H., Siddiqui K. S. (2016). Lignocellulosic biomass: biosynthesis, degradation and industrial utilization. Eng. Life Sci. 16, 1–16. 10.1002/elsc.201400196 [DOI] [Google Scholar]
  24. Guerriero G., Sergeant K., Hausman J. F. (2014). Wood biosynthesis and typologies: a molecular rhapsody. Tree Physiol. 34, 839–855. 10.1093/treephys/tpu031 [DOI] [PubMed] [Google Scholar]
  25. Guo F. Q., Young J., Crawford N. M. (2003). The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell. 15, 107–117. 10.1105/tpc.006312 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hong M. J., Kim D. Y., Lee T. G., Jeon W. B., Seo Y. W. (2010). Functional characterization of pectin methylesterase inhibitor (PMEI) in wheat. Genes Genet. Syst. 85, 97–106. 10.1266/ggs.85.97 [DOI] [PubMed] [Google Scholar]
  27. Hsu P. K., Tsay Y. F. (2013). Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributingxylem-borne nitrate to enhance plant growth. Plant Physiol. 163, 844–856. 10.1104/pp.113.226563 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hu R., Zhu Y., Wei J., Chen J., Shi H., Shen G., et al. (2017). Overexpression of PP2A-C5 that encodes the catalytic subunit 5 of protein phosphatase 2A in Arabidopsis confers better root and shoot development under salt conditions. Plant Cell Environ. 40, 150–164. 10.1111/pce.12837 [DOI] [PubMed] [Google Scholar]
  29. Iovieno P., Punzo P., Guida G., Mistretta C., Van Oosten M. J., Nurcato R., et al. (2011). Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front. Plant Sci. 7:371. 10.3389/fpls.2016.00371 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kiba T., Krapp A. (2016). Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol. 57, 707–714. 10.1093/pcp/pcw052 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Landi S., De Lillo A., Nurcato R., Grillo S., Esposito S. (2017a). In-field study on traditional Italian tomato landraces: the constitutive activation of ROS scavenging machinery reduces effects of drought stress. Plant Physiol. Biochem. 118, 150–160. 10.1016/j.plaphy.2017.06.011 [DOI] [PubMed] [Google Scholar]
  32. Landi S., Hausman J. F., Guerriero G., Esposito S. (2017b). Poaceae vs abiotic stress: focus on drought and salt stress, recent insights and perspectives. Front. Plant Sci. 8:1214. 10.3389/fpls.2017.01214 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Leucci M. R., Lenucci M. S., Piro G., Dalessandro G. (2008). Water stress and cell wall polysaccharides in the apical root zone of wheat cultivars varying in drought tolerance. J. Plant Physiol. 165, 1168–1180. 10.1016/j.jplph.2007.09.006 [DOI] [PubMed] [Google Scholar]
  34. Li G., Tillard P., Gojon A., Maurel C. (2016). Dual regulation of root hydraulic conductivity and plasma membrane aquaporins by plant nitrate accumulation and high-affinity nitrate transporter NRT2.1. Plant Cell Physiol. 57, 733–742. 10.1093/pcp/pcw022 [DOI] [PubMed] [Google Scholar]
  35. Li X., Zhao J., Walk T. C., Liao H. (2014). Characterization of soybean β-expansin genes and their expression responses to symbiosis, nutrient deficiency and hormone treatment. Appl. Microbiol. Biotechnol. 98, 2805–2817. 10.1007/s00253-013-5240-z [DOI] [PubMed] [Google Scholar]
  36. Li Y., Huang J., Song X., Zhang Z., Jiang Y., Zhu Y., et al. (2017). An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant. Planta 246, 91–103. 10.1007/s00425-017-2688-6 [DOI] [PubMed] [Google Scholar]
  37. Ma C., Haslbeck M., Babujee L., Jahn O., Reumann S. (2006). Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol. 141, 47–60. 10.1104/pp.105.073841 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Marín-Rodríguez M. C., Orchard J., Seymour G. B. (2002). Pectate lyases, cell wall degradation and fruit softening. J. Exp. Bot. 53, 2115–2119. 10.1093/jxb/erf089 [DOI] [PubMed] [Google Scholar]
  39. Marowa P., Ding A., Kong Y. (2016). Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep. 35, 949–965. 10.1007/s00299-016-1948-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Minoia S., Boualem A., Marcel F., Troadec C., Quemener B., Cellini F., et al. (2015). Induced mutations in tomato SlExp1 alter cell wall metabolism and delay fruit softening. Plant Sci. 242, 1–8. 10.1016/j.plantsci.2015.07.001 [DOI] [PubMed] [Google Scholar]
  41. Quan X., Zeng J., Ye L., Chen G., Han Z., Munawar J., et al. (2016). Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen. BMC Plant Biol. 16:30. 10.1186/s12870-016-0721-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reynolds M., Tuberosa R. (2008). Translational research impacting on crop productivity in drought-prone environments. Curr. Opin. Plant Biol. 11, 171–179. 10.1016/j.pbi.2008.02.005 [DOI] [PubMed] [Google Scholar]
  43. Ruggiero A., Punzo P., Landi S., Costa A., Van Ooosten M., Grillo S. (2017). Improving plant water use efficiency through molecular genetics. Horticulturae 3:31 10.3390/horticulturae3020031 [DOI] [Google Scholar]
  44. Sun L., Nocker S. (2010). Analysis of promoter activity of members of the PECTATE LYASE-LIKE (PLL) gene family in cell separation in Arabidopsis. BMC Plant Biol. 10:152. 10.1186/1471-2229-10-152 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tenhaken R. (2015). Cell wall remodeling under abiotic stress. Front. Plant Sci. 5:771. 10.3389/fpls.2014.00771 [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Van Oosten M., Costa A., Punzo P., Landi S., Ruggiero A., Batelli G., et al. (2016). Genetics of drought stress tolerance in crop plants, in Drought Stress Tolerance in Plants Vol. 2, eds Hossain M. A., Wani S. H., Bhattachajee S., Burrit D., Phan tran L. (Berlin: Springer; ), 39–70. [Google Scholar]
  47. Weichert A., Brinkmann C., Komarova N. Y., Dietrich D., Thor K., Meier S., et al. (2012). AtPTR4 and AtPTR6 are differentially expressed, tonoplast-localized members of the peptide transporter/nitrate transporter 1 (PTR/NRT1) family. Planta 235, 311–323. 10.1007/s00425-011-1508-7 [DOI] [PubMed] [Google Scholar]
  48. Yamaji N., Huang C. F., Nagao S. (2009). A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21, 3339–3349. 10.1105/tpc.109.070771 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yang W., Yoon J., Choi H., Fan Y., Chen R., An G. (2015). Transcriptome analysis of nitrogen-starvation-responsive genes in rice. BMC Plant Biol. 15:31. 10.1186/s12870-015-0425-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zhao W., Yang X., Yu H., Jiang W., Sun N., Liu X., et al. (2015). RNA-Seq-based transcriptome profiling of early nitrogen deficiency response in cucumber seedlings provides new insight into the putative nitrogen regulatory network. Plant Cell Physiol. 56, 455–467. 10.1093/pcp/pcu172 [DOI] [PubMed] [Google Scholar]
  51. Zhou J., Xie J., Liao H., Wang X. (2014). Overexpression of b-expansin gene GmEXPB2 improves phosphorus efficiency in soybean. Physiol. Plant. 150, 194–204. 10.1111/ppl.12077 [DOI] [PubMed] [Google Scholar]

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