Physiological and molecular bases of the boron deficiency response in tomatoes

Junjun Li , Huihui Fan , Qianqian Song , Lili Jing , Hao Yu , Ruishan Li , Ping Zhang , Fei Liu , Weimin Li , Liangliang Sun , Jin Xu

Horticulture Research ›› 2023, Vol. 10 ›› Issue (12) : 229

PDF (4468KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (12) :229 DOI: 10.1093/hr/uhad229
Article
research-article
Physiological and molecular bases of the boron deficiency response in tomatoes
Author information +
History +
PDF (4468KB)

Abstract

Boron is an essential microelement for plant growth. Tomato is one of the most cultivated fruits and vegetables in the world, and boron deficiency severely inhibits its yield and quality. However, the mechanism of tomato in response to boron deficiency remains largely unclear. Here, we investigated the physiological and molecular bases of the boron deficiency response in hydroponically grown tomato seedlings. Boron deficiency repressed the expression of genes associated with nitrogen metabolism, while it induced the expression of genes related to the pentose phosphate pathway, thereby altering carbon flow to provide energy for plants to cope with stress. Boron deficiency increased the accumulation of copper, manganese and iron, thereby maintaining chlorophyll content and photosynthetic efficiency at the early stage of stress. In addition, boron deficiency downregulated the expression of genes involved in cell wall organization and reduced the contents of pectin and cellulose in roots, ultimately retarding root growth. Furthermore, boron deficiency markedly altered phytohormone levels and signaling pathways in roots. The contents of jasmonic acid, jasmonoy1-L-isoleucine, trans-zeatin riboside, abscisic acid, salicylic acid, and SA glucoside were decreased; in contrast, the contents of isopentenyladenine riboside and ethylene precursor 1-aminocyclopropane-1-carboxylic acid were increased in the roots of boron-deficient tomato plants. These results collectively indicate that tomato roots reprogram carbon/nitrogen metabolism, alter cell wall components and modulate phytohormone pathways to survive boron deficiency. This study provides a theoretical basis for further elucidating the adaptive mechanism of tomato in response to boron deficiency.

Cite this article

Download citation ▾
Junjun Li, Huihui Fan, Qianqian Song, Lili Jing, Hao Yu, Ruishan Li, Ping Zhang, Fei Liu, Weimin Li, Liangliang Sun, Jin Xu. Physiological and molecular bases of the boron deficiency response in tomatoes. Horticulture Research, 2023, 10 (12) : 229 DOI:10.1093/hr/uhad229

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This research was supported by the China National Natural Sciences Foundation (32070314) to J.X., the Science and Technology Innovation Fund project of Shanxi Agricultural University (2020BQ24) to P.Z., and the Basic Research Program of Shanxi Province (Free Exploration) (20210302124369) to L.S.

Author contributions

J.L.: investigation, data curation, formal analysis, visualization, writing-original draft, writing-review & editing. H.F.: investigation, visualization. L.J.: investigation, visualization. P.Z.: methodology, conceptualization. F.L.: methodology. L.S.: methodology. H.Y.: investigation. Q.S.: investigation. R.L.: investigation. W.L.: investigation. J.X.: Writing-review & editing, supervision, conceptualization, methodology, validation, supervision, project administration.

Data availability

The raw data of RNA-seq were archived at the SRA of NCBI under accession no. PRJNA910924.

Conflict of interest

The authors have no conflict of interest to declare.

References

[1]

Blevins DG, Lukaszewski KM . Boron in plant structure and function. Annu Rev Plant Biol. 1998; 49: 481-500

[2]

Brdar-Jokanović M . Boron toxicity and deficiency in agricultural plants. Int J Mol Sci. 2020; 21: 1424

[3]

Shorrocks VM . The occurrence and correction of boron deficiency. Plant Soil. 1997; 193: 121-48

[4]

Uraguchi S, Kato Y, Hanaoka H, et al. Generation of boron-deficiency-tolerant tomato by overexpressing an Arabidopsis thaliana borate transporter AtBOR1. Front Plant Sci. 2014; 5: 125

[5]

Tanaka M, Wallace IS, Takano J, et al. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell. 2008; 20: 2860-75

[6]

Zhao D, Oosterhuis DM . Cotton growth and physiological responses to boron deficiency. J Plant Nutr. 2003; 26: 855-67

[7]

Reid R. Understanding the boron transport network in plants. Plant Soil. 2014; 385: 1-13

[8]

O’Neill MA, Eberhard S, Albersheim P, et al. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science. 2001; 294: 846-9

[9]

Takano J, Miwa K, Fujiwara T . Boron transport mechanisms: collaboration of channels and transporters. Trends Plant Sci. 2008; 13: 451-7

[10]

Takano J, Tanaka M, Toyoda A, et al. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci. 2010; 107: 5220-5

[11]

Takano J, Noguchi K, Yasumori M, et al. Arabidopsis boron transporter for xylem loading. Nature. 2002; 420: 337-40

[12]

Miwa K, Wakuta S, Takada S, et al. Roles of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation under boron limitation in Arabidopsis. Plant Physiol. 2013; 163: 1699-709

[13]

Li X, Li Y, Mai J, et al. Boron alleviates aluminum toxicity by promoting root alkalization in transition zone via polar auxin transport. Plant Physiol. 2018; 177: 1254-66

[14]

Chen X, Smith SM, Shabala S, et al. Phytohormones in plant responses to boron deficiency and toxicity. J Exp Bot. 2023; 74: 743-54

[15]

Li L, Verstraeten I, Roosjen M, et al. Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature. 2021; 599: 273-7

[16]

Oiwa Y, Kitayama K, Kobayashi M, et al. Boron deprivation immediately causes cell death in growing roots of Arabidopsis thaliana (L.) Heynh. Soil Sci Plant Nutr. 2013; 59: 621-7

[17]

Huang Y, Wang S, Wang C, et al. Induction of jasmonic acid biosynthetic genes inhibits Arabidopsis growth in response to low boron. J Integr Plant Biol. 2021; 63: 937-48

[18]

Zhang C, He M, Wang S, et al. Boron deficiency-induced root growth inhibition is mediated by brassinosteroid signalling regulation in Arabidopsis. Plant J. 2021; 107: 564-78

[19]

Poza-Viejo L, Abreu I, González-García MP, et al. Boron deficiency inhibits root growth by controlling meristem activity under cytokinin regulation. Plant Sci. 2018; 270: 176-89

[20]

Li N, He Q, Wang J, et al. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nat Genet. 2023; 55: 852-60

[21]

Bohnsack CW, Albert LS . Early effects of boron deficiency on indoleacetic acid oxidase levels of squash root tips. Plant Physiol. 1977; 59: 1047-50

[22]

Wang Y, Zhao Z, Wang S, et al. Boron mediates nitrogen starvation-induced leaf senescence by regulating ROS production and C/N balance in Brassica napus. Environ Exp Bot. 2022; 200: 104905

[23]

Mukhopadhyay M, Ghosh PD, Mondal TK . Effect of boron deficiency on photosynthesis and antioxidant responses of young tea plantlets. Russ J Plant Physiol. 2013; 60: 633-9

[24]

Song X, Song B, Huo J, et al. Effect of boron deficiency on the photosynthetic performance of sugar beet cultivars with contrasting boron efficiencies. Front Plant Sci. 2023; 13: 1101171

[25]

Wolters H, Jürgens G . Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet. 2009; 10: 305-17

[26]

Tao L, Zhu H, Huang Q, et al. PIN2/3/4 auxin carriers mediate root growth inhibition under conditions of boron deprivation in Arabidopsis. Plant J. 2023; 115: 1357-76

[27]

Feng Y, Cui R, Wang S, et al. Transcription factor BnaA9.WRKY47 contributes to the adaptation of Brassica napus to low boron stress by up-regulating the boric acid channel gene BnaA3.NIP5;1. Plant Biotechnol J. 2020; 18: 1241-54

[28]

Hua Y, Zhang D, Zhou T, et al. Transcriptomics-assisted quantitative trait locus fine mapping for the rapid identification of a nodulin 26-like intrinsic protein gene regulating boron efficiency in allotetraploid rapeseed. Plant Cell Environ. 2016; 39: 1601-18

[29]

Takei K, Yamaya T, Sakakibara H . Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J Biol Chem. 2004; 279: 41866-72

[30]

Schomburg FM, Bizzell CM, Lee DJ, et al. Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell. 2003; 15: 151-63

[31]

Reinecke DM, Wickramarathna AD, Ozga JA, et al. Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol. 2013; 163: 929-45

[32]

Durand C, Vicré-Gibouin M, Follet-Gueye ML, et al. The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol. 2009; 150: 1411-21

[33]

Milagres CDC, Maia JTLS, Ventrella MC, et al. Anatomical changes in cherry tomato plants caused by boron deficiency. Braz J Bot. 2019; 42: 319-28

[34]

El-Shintinawy F . Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynthetica. 2000; 36: 565-73

[35]

Han S, Chen LS, Jiang HX, et al. Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol. 2008; 165: 1331-41

[36]

Xin W, Zhang L, Zhang W, et al. An integrated analysis of the rice transcriptome and metabolome reveals differential regulation of carbon and nitrogen metabolism in response to nitrogen availability. Int J Mol Sci. 2019; 20: 2349

[37]

Lu YB, Yang LT, Li Y, et al. Effects of boron deficiency on major metabolites, key enzymes and gas exchange in leaves and roots of Citrus sinensis seedlings . Tree Physiol. 2014; 34: 608-18

[38]

Kaur H, Kaur H, Kaur H, et al. The beneficial roles of trace and ultratrace elements in plants. Plant Growth Regul. 2023; 100: 219-36

[39]

Ruiz JM, Baghour M, Bretones G, et al. Nitrogen metabolism in tobacco plants (Nicotiana tabacum L.): role of boron as a possible regulatory factor . Int J Plant Sci. 1998; 159: 121-6

[40]

Ramón AM, Ruiz ROC, Gárate A . In vitro stabilization and distribution of nitrate reductase in tomato plants. Incidence of boron deficiency. J Plant Physiol. 1989; 135: 126-8

[41]

Yang H, Menz J, Häussermann I, et al. High and low affinity urea root uptake: involvement of NIP5;1. Plant Cell Physiol. 2015; 56: 1588-97

[42]

Gu R, Chen X, Zhou Y, et al. Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport. BMB Rep. 2012; 45: 96-101

[43]

Zhang L, Yan J, Vatamaniuk OK, et al. CsNIP2;1 is a plasma membrane transporter from Cucumis sativus that facilitates urea uptake when expressed in Saccharomyces cerevisiae and Arabidopsis thaliana. Plant Cell Physiol. 2016; 57: 616-29

[44]

Pang Y, Li L, Ren F, et al. Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics. 2010; 37: 389-97

[45]

Eide D, Broderius M, Fett J, et al. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci. 1996; 93: 5624-8

[46]

Thomine S, Wang R, Ward JM, et al. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci. 2000; 97: 4991-6

[47]

Kato T, Kumazaki K, Wada M, et al. Crystal structure of plant vacuolar iron transporter VIT1. Nat Plants. 2019; 5: 308-15

[48]

Ricachenevsky FK, Menguer PK, Sperotto RA, et al. Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front Plant Sci. 2013; 4: 144

[49]

Sanz A, Pike S, Khan MA, et al. Copper uptake mechanism of Arabidopsis thaliana high-affinity COPT transporters . Protoplasma. 2019; 256: 161-70

[50]

Curie C, Cassin G, Couch D, et al. Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot. 2009; 103: 1-11

[51]

Alejandro S, Höller S, Meier B, et al. Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci. 2020; 11: 300

[52]

Mir AR, Alam P, Hayat S . Auxin regulates growth, photosynthetic efficiency and mitigates copper induced toxicity via modulation of nutrient status, sugar metabolism and antioxidant potential in Brassica juncea. Plant Physiol Biochem. 2022; 185: 244-59

[53]

Ahmad S, Hussain N, Ahmed N, et al. Influence of boron nutrition on physiological parameters and productivity of cotton (Gossypium hirsutum L.) crop . Pak J Bot. 2019; 51: 401-08

[54]

Chen M, Mishra S, Heckathorn SA, et al. Proteomic analysis of Arabidopsis thaliana leaves in response to acute boron deficiency and toxicity reveals effects on photosynthesis, carbohydrate metabolism, and protein synthesis . J Plant Physiol. 2014; 171: 235-42

[55]

Wu X, Riaz M, Yan L, et al. Boron deficiency in trifoliate orange induces changes in pectin composition and architecture of components in root cell walls. Front Plant Sci. 2017; 8: 1882

[56]

Song X, Song B, Huo J, et al. Boron-efficient sugar beet (Beta vulgaris l.) cultivar improves tolerance to boron deficiency by improving leaf traits . J Soil Sci Plant Nutr. 2022; 22: 4217-27

[57]

Pommerrenig B, Junker A, Abreu I, et al. Identification of rapeseed (Brassica napus) cultivars with a high tolerance to boron-deficient conditions . Front Plant Sci. 2018; 9: 1142

[58]

Abreu I, Poza L, Bonilla I, et al. Boron deficiency results in early repression of a cytokinin receptor gene and abnormal cell differentiation in the apical root meristem of Arabidopsis thaliana. Plant Physiol Biochem. 2014; 77: 117-21

[59]

Kiba T, Takei K, Kojima M, et al. Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev Cell. 2013; 27: 452-61

[60]

Herrera-Rodríguez MB, Camacho-Cristóbal JJ, Barrero-Rodríguez R, et al. Crosstalk of cytokinin with ethylene and auxin for cell elongation inhibition and boron transport in Arabidopsis primary root under boron deficiency. Plan Theory. 2022; 11: 2344

[61]

Zhou T, Hua Y, Huang Y, et al. Physiological and transcriptional analyses reveal differential phytohormone responses to boron deficiency in Brassica napus genotypes . Front Plant Sci. 2016; 7: 221

[62]

Maurer F, Müller S, Bauer P . Suppression of Fe deficiency gene expression by jasmonate. Plant Physiol Biochem. 2011; 49: 530-6

[63]

Cui Y, Chen CL, Cui M, et al. Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis. Mol Plant. 2018; 11: 1166-83

[64]

Agami RA, Mohamed GF . Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf. 2013; 94: 164-71

[65]

Du C, Zhao P, Zhang H, et al. The Reaumuria trigyna transcription factor RtWRKY1 confers tolerance to salt stress in transgenic Arabidopsis. J Plant Physiol. 2017; 215: 48-58

[66]

Chen T, Zhang B . Measurements of proline and malondialdehyde content and antioxidant enzyme activities in leaves of drought stressed cotton. Bio-protocol. 2016; 6: e1913-3

[67]

Elavarthi S, Martin B . Spectrophotometric assays for antioxidant enzymes in plants. Methods Mol Biol. 2010; 639: 273-81

[68]

Wei K, Jin X, Chen X, et al. The effect of H2O2 and abscisic acid (ABA) interaction on β-amylase activity under osmotic stress during grain development in barley . Plant Physiol Biochem. 2009; 47: 778-84

[69]

Zeng P, Huang F, Guo Z, et al. Physiological responses of Morus alba L. in heavy metal (loid)-contaminated soil and its associated improvement of the microbial diversity . Environ Sci Pollut Res. 2020; 27: 4294-308

[70]

Liu YY, Wang RL, Zhang P, et al. Involvement of reactive oxygen species in lanthanum-induced inhibition of primary root growth. J Exp Bot. 2016; 67: 6149-59

[71]

Šimura J, Antoniadi I, Široká J, et al. Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 2018; 177: 476-89

[72]

Xin P, Guo Q, Li B, et al. A tailored high-efficiency sample pretreatment method for simultaneous quantification of 10 classes of known endogenous phytohormones. Plant Commun. 2020; 1: 100047

[73]

Meng LS, Xu MK, Li D, et al. Soluble sugar accumulation can influence seed size via AN3-YDA gene cascade. J Agric Food Chem. 2017; 65: 4121-32

[74]

Love MI, Huber W, Anders S . Moderated estimation of fold change and dispersion for rna-seq data with deseq2. Genome Biol. 2014; 15: 550

[75]

Hu H, Brown PH . Localization of boron in cell walls of squash and tobacco and its association with pectin (evidence for a structural role of boron in the cell wall). Plant Physiol. 1994; 105: 681-9

[76]

Blumenkrantz N, Asboe-Hansen G . New method for quantitative determination of uronic acids. Anal Biochem. 1973; 54: 484-9

PDF (4468KB)

85

Accesses

0

Citation

Detail

Sections
Recommended

/