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Boron-Efficient Sugar Beet (Beta vulgaris L.) Cultivar Improves Tolerance to Boron Deficiency by Improving Leaf Traits

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Abstract

Crop nutrient-efficient cultivars are more adapted to the nutrient-deficient environment. However, the physiological tolerance mechanisms of boron (B)-efficient sugar beet cultivars in response to B deficiency are unclear. Therefore, the B-efficient and B-inefficient sugar beet cultivars were used as test materials and cultured at two B levels (B deficiency and normal) to investigate the changes in the sugar beet leaf morphology, cell wall composition, and related gene expression under B-deficient conditions. The results indicated that B deficiency distorted the cell wall structure, altered cell wall components, and adversely affected leaf morphology. However, compared with the B-inefficient cultivar, the B-efficient sugar beet cultivar allocated more B concentration in the cell wall under B-deficient conditions. In B-efficient sugar beet cultivar leaves, the chelator-soluble pectin contents were remarkably increased while the alkali-soluble pectin content decreased, and the KDOPS expression was less upregulated. The B-efficient sugar beet cultivar accumulated more leaf biomass, a larger leaf area, and was less affected by B deprivation. In conclusion, the B-efficient cultivar responded efficiently in cell wall composition, gene expression, and leaf morphology, thus demonstrating better resistance to B-deficient stress.

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References

  • Chormova D, Messenger DJ, Fry SC (2014a) Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion. Plant J 77:534–546

    Article  CAS  PubMed  Google Scholar 

  • Chormova D, Messenger DJ, Fry SC (2014b) Rhamnogalacturonan-II cross-linking of plant pectins via boron bridges occurs during polysaccharide synthesis and secretion. Plant Signal Behav 9(3):e28169

    Article  PubMed  PubMed Central  Google Scholar 

  • Cong RH, Wang Y, Li XK, Ren T, Lu JW (2020) Differential responses of seed yield and yield components to nutrient deficiency between direct sown and transplanted winter Oilseed Rape. Int J Plant Prod 14:77–92

    Article  Google Scholar 

  • Cong XL, Jing HY, Lin N, Xia ZH, Huang MJ, Jiang XY (2015) Boron deficiency affects cell morphology and structure of young leaves of radish. Acta Physiol Plant 37:247–257

    Article  Google Scholar 

  • Dannel F, Pfeffer H, Romheld V (1998) Compartmentation of boron in roots and leaves of sunflower as affected by boron supply. J Plant Physiol 153:615–622

    Article  CAS  Google Scholar 

  • Dinh AQ, Naeem A, Sagervanshi A, Wimmer MA, Muhling KH (2021) Boron uptake and distribution by oilseed rape (Brassica napus L.) as affected by different nitrogen forms under low and high boron supply. Plant Physiol Biochem 161:156–165

    Article  CAS  PubMed  Google Scholar 

  • Dong XC, Lu XP, Wu XW, Liu GD, Yan L, Muhammad R, Wu LS, Jiang CC (2018) Changes in chemical composition and structure of root cell wall of citrus rootstock seedlings in response to boron deficiency by FTIR spectroscopy. J Hortic Sci Biotechnol 93:150–158

    Article  CAS  Google Scholar 

  • Du CW, Wang YH, Xu FS, Yang YH, Wang HY (2006) Study on the physiological mechanism of boron utilization efficiency in rape cultivars. J Plant Nutr 25:231–244

    Article  Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (2002) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  Google Scholar 

  • Gotz LF, Silvestrin F, Motta ACV, Pauletti V (2021) Response to application and tissue diagnosis of boron deficiency and toxicity in maize. Commun Soil Sci Plant Anal 52:2898–2911

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. The College of Agriculture University of California, Berkeley

    Google Scholar 

  • Ishii T, Matsunaga T, Pellerin P, O’Neill MA, Darvill A, Albersheim P (1999) The plant cell wall polysaccharide Rhamnogalacturonan II self-assembles into a covalently cross-linked dimer. J Biol Chem 274:13098–13104

    Article  CAS  PubMed  Google Scholar 

  • Kelly JF, Gabelman WH (1960) Variability in of varieties and strains of red beets (Beta vulgaris L.) boron. Proc Amer Soc Hort Sci 76:409–415

    CAS  Google Scholar 

  • Kong JL, Yu SN (2007) Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sin 39:549–559

    Article  CAS  PubMed  Google Scholar 

  • Läuchli A (2002) Functions of boron in higher plants: recent advances and open questions. Plant Biol 4:190–192

    Article  Google Scholar 

  • Li XW, Liu JY, Fang J, Tao L, Shen RF, Li YL, Xiao HD, Feng YM, Wen HX, Guan JH, Wu LS, He YM, Goldbach HE, Yu M (2017) Boron supply enhances aluminum tolerance in root border cells of pea (Pisum sativum) by interacting with cell wall pectins. Front Plant Sci 8:742–753

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu GD, Jiang CC, Wang YH (2011) Distribution of boron and its forms in young “Newhall” navel orange (Citrus sinensis Osb) plants grafted on two rootstocks in response to deficient and excessive boron. Soil Sci Plant Nutr 57:93–104

    Article  CAS  Google Scholar 

  • Liu GD, Dong XC, Liu LC, Wu LS, Peng SA, Jiang CC (2014) Boron deficiency is correlated with changes in cell wall structure that lead to growth defects in the leaves of navel orange plants. Sci Hortic 176:54–62

    Article  CAS  Google Scholar 

  • Liu GD, Wang RD, Liu LC, Wu LS, Jiang CC (2013) Cellular boron allocation and pectin composition in two citrus rootstock seedlings differing in boron-deficiency response. Plant Soil 370:555–565

    Article  CAS  Google Scholar 

  • Liu GD, Wang RD, Wu LS, Peng SA, Wang YH, Jiang CC (2015) Differential changes in cell-wall content and boron and calcium concentration in newhall navel orange grafted on two rootstocks differing in boron-deficiency responses. Commun Soil Sci Plant Anal 46:439–453

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Loomis WD, Durst RW (1992) Chemistry and biology of boron. BioFactors 3:229–239

    CAS  PubMed  Google Scholar 

  • Mesquita GL, Zambrosi FC, Tanaka FA, Boaretto RM, Quaggio JA, Ribeiro RV, Mattos D (2016) Anatomical and physiological responses of citrus trees to varying boron availability are dependent on rootstock. Front Plant Sci 7:224–236

    Article  PubMed  PubMed Central  Google Scholar 

  • Milagres CC, Maia JTLS, Ventrella MC, Martinez HEP (2019) Anatomical changes in tomato plants caused by boron deficiency. Braz J Bot 42:319–328

    Article  Google Scholar 

  • Mishra S, Heckathorn SA, Frantz JM, Krause C (2018) The effect of boron availability, CO2, and irradiance on relative accumulation of the major boron transport proteins, BOR1 and NIP5;1 Biol Plant 62:121–128

    Article  CAS  Google Scholar 

  • Monteiro F, Frese L, Castro S, Duarte MC, Paulo OS, Loureiro J, Romeiras MM (2018) Genetic and genomic tools to asssist sugar beet improvement: the value of the crop wild relatives. Front Plant Sci 9:74–82

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849

    Article  PubMed  Google Scholar 

  • O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 271:22923–22930

    Article  PubMed  Google Scholar 

  • Ouadah O, Merad G, Saidi F, Mendi S, Dergal M (2020) Influence of alloying transition metals on structural, elastic, electronic and optical behaviors of γ-TiAl based alloys: a comparative DFT study combined with data mining technique. Mater Chem Phys 242:122455

    Article  CAS  Google Scholar 

  • Pan Y, Wang ZH, Yang L, Wang ZF, Shi L, Naran R, Azadi P, Xu FS (2012) Differences in cell wall components and allocation of boron to cell walls confer variations in sensitivities of Brassica napus cultivars to boron deficiency. Plant Soil 354:383–394

    Article  CAS  Google Scholar 

  • Pommerrenig B, Junker A, Abreu I, Bieber A, Fuge J, Willner E, Bienert MD, Altmann T, Bienert GP (2018) Identification of rapeseed (Brassica napus) cultivars with a high tolerance to boron-deficient conditions. Front Plant Sci 9:1142–1164

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin SY, Xu YF, Liu HE, Li C, Yang Y, Zhao P (2021) Effect of different boron levels on yield and nutrient content of wheat based on grey relational degree analysis. Acta Physiol Plant 43:127–135

    Article  CAS  Google Scholar 

  • Riaz M, Yan L, Wu XW, Hussain S, Aziz O, Jiang CC (2018) Boron induced inhibition of root elongation is provoked by oxidative damage, root injuries and changes in cell wall structure. Environ Exp Bot 156:74–85

    Article  CAS  Google Scholar 

  • Riaz M, Kamran M, El-Esawi MA, Hussain S, Wang X (2021a) Boron-toxicity induced changes in cell wall components, boron forms, and antioxidant defense system in rice seedlings. Ecotoxicol Environ Saf 216:112192

    Article  CAS  PubMed  Google Scholar 

  • Riaz M, Kamran M, Fang Y, Yang G, Rizwan M, Ali S, Zhou Y, Wang Q, Deng L, Wang Y, Wang X. (2021b) Boron supply alleviates cadmium toxicity in rice (Oryza sativa L.) by enhancing cadmium adsorption on cell wall and triggering antioxidant defense system in roots. Chemosphere 266:128938

  • Riaz M, Kamran M, Rizwan M, Ali S, Wang X (2022) Foliar application of silica sol alleviates boron toxicity in rice (Oryza sativa) seedlings. J Hazard Mater 423:127175

    Article  CAS  PubMed  Google Scholar 

  • Ruiz M, Quinones A, Martinez-Alcantara B, Aleza P, Morillon R, Navarro L, Primo-Millo E, Martinez-Cuenca MR (2016) Tetraploidy enhances boron-excess tolerance in carrizo citrange (Citrus sinensis L. Osb. x Poncirus trifoliata L. Raf.). Front Plant Sci 7:701–717

    Article  PubMed  PubMed Central  Google Scholar 

  • Saidi F, Khetari S, Yahia IS, Zahran HY, Hidouri T, Ameur N (2022) The use of principal component analysis (PCA) and partial least square (PLS) for designing new hard inverse perovskites materials. Condens Matter Syst 31:e00667

    Google Scholar 

  • Scott L (1941) In an instance of boron in the grape under field conditions. Proc Amer Soc Hort Sci 38:375–378

    CAS  Google Scholar 

  • Shi L, Wang YH, Nian NZ, Lu JW, Meng JL, Xu FS (2009) Inheritance of boron efficiency in oilseed rape. Pedosphere 19:403–408

    Article  CAS  Google Scholar 

  • Shireen F, Nawaz MA, Chen C, Zhang QK, Zheng ZH, Sohail H, Sun JY, Cao HS, Huang Y, Bie ZL (2018) Boron: Functions and approaches to enhance its availability in plants for sustainable agriculture. Int J Mol Sci 19:1856–1876

    Article  PubMed  PubMed Central  Google Scholar 

  • Shireen F, Nawaz MA, Lu J, Xiong M, Kaleem M, Huang Y, Bie Z (2021) Application of boron reduces vanadium toxicity by altering the subcellular distribution of vanadium, enhancing boron uptake and enhancing the antioxidant defense system of watermelon. Ecotoxicol Environ Saf 226:112828

    Article  CAS  PubMed  Google Scholar 

  • Song BQ, Hao XM, Wang XL, Yang SY, Dong YF, Ding Y, Wang QH, Wang XC, Zhou JC (2019) Boron stress inhibits beet (Beta vulgaris L.) growth through influencing endogenous hormones and oxidative stress response. Soil Sci Plant Nutr 65:346–352

    Article  Google Scholar 

  • Song X, Hao XM, Song BQ, Zhao XY, Wu ZZ, Wang X, Du JY, Huang WG, Riaz M, Li XF, Li JX, Li MY, Zhang X (2021a) The oxidative damage and morphological changes of sugar beet (Beta vulgaris L.) leaves at seedlings stage exposed to boron deficiency in hydroponics. Sugar Tech 24:532–541

    Article  Google Scholar 

  • Song X, Wang XL, Song BQ, Wu ZZ, Zhao XY, Huang WG, Riaz M (2021b) Transcriptome analysis reveals the molecular mechanism of boron deficiency tolerance in leaves of boron-efficient Beta vulgaris seedlings. Plant Physiol Biochem 168:294–304

    Article  CAS  PubMed  Google Scholar 

  • Spurr AR (1957) The effect of boron on cell-wall structure in celery. Am J Bot 44(8):637–650

    Article  CAS  Google Scholar 

  • Tripathi P, Singh RP, Srivastava S, Shivanna B, Singh AK, Singh S, Khare P (2021) Quantifying the boron demand of Pelargonium graveolens for optimum biomass yield and quality of essential oil under field conditions. J Plant Nutr 45:218–231

    Article  Google Scholar 

  • Verma RK, Singh S, Verma RB, Singh MP, Kumar V (2021) Effect of Boron (B) and Zinc (Zn) on the yield and attributing characters of cauliflower. Natl Acad Sci Lett 44:369–371

    Article  CAS  Google Scholar 

  • Wei R, Huang M, Huang D, Zhou JZ, Pan XJ, Zhang WE (2022) Growth, gas exchange, and boron distribution characteristics in two grape species plants under boron deficiency condition. Horticulturae 8:374

    Article  Google Scholar 

  • Wu XW, Riaz M, Yan L, Du CQ, Liu YL, Jiang CC (2017) Boron deficiency in trifoliate orange induces changes in pectin composition and architecture of components in root cell walls. Front Plant Sci 8:1882–1892

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu ZZ, Wang XL, Song BQ, Zhao XY, Du JY, Huang WG (2021) Responses of photosynthetic performance of sugar beet varieties to foliar boron spraying. Sugar Tech 23:1332–1339

    Article  CAS  Google Scholar 

  • Xu W, Wang P, Yuan L, Chen X, Hu X (2021) Effects of application methods of boron on tomato growth, fruit quality and flavor. Horticulturae 7:223–235

    Article  Google Scholar 

  • Xue J, Lin M, Bell RW, Graham RD, Yang X, Yang Y (1998) Differential response of oilseed rape (Brassica napus L.) cultivars to low boron supply. Plant Soil 204:155–163

    Article  CAS  Google Scholar 

  • Yamuangmorn S, Laororng K, Saenchai C, Lordkaew S, Dell B, Prom-U-Thai C (2021) Boron requirement for vegetative growth of Sacha inchi (Plukentia volubilis L.). J Plant Nutr 45:845–853

    Article  Google Scholar 

  • Yan L, Riaz M, Wu XW, Du CQ, Liu YL, Jiang CC (2018) Ameliorative effects of boron on aluminum induced variations of cell wall cellulose and pectin components in trifoliate orange (Poncirus trifoliate (L.) Raf.) rootstock. Environ Pollut 240:764–774

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Li S, Riaz M, Jiang CC (2021a) Proline metabolism and biosynthesis behave differently in response to boron-deficiency and toxicity in Brassica napus. Plant Physiol Biochem 167:529–540

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Riaz M, Liu JY, Liu YL, Zeng Y, Jiang CC (2021b) Boron reduces aluminum deposition in alkali-soluble pectin and cytoplasm to release aluminum toxicity. J Hazard Mater 401:123388

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Riaz M, Cheng J, Jiang CC (2022) Boron-deficiency and aluminum toxicity activate antioxidant defense and disorganize the cell wall composition and architecture in trifoliate orange leaf. Sci Hortic 297:110961

    Article  CAS  Google Scholar 

  • Yin Q, Kang L, Liu Y, Qaseem MF, Qin W, Liu T, Li H, Deng X, Wu AM (2022) Boron deficiency disorders the cell wall in Neolamarckia cadamba Ind Crops Prod 176:114332

    Article  CAS  Google Scholar 

  • Zhang C, He M, Jiang Z, Liu L, Pu J, Zhang W, Wang S, Xu F (2022) The xyloglucan endotransglucosylase/hydrolase gene XTH22/TCH4 regulates plant growth by disrupting the cell wall homeostasis in arabidopsis under boron deficiency. Int J Mol Sci 23:1250–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang DD, Zhao H, Shi L, Xu FS (2014) Physiological and genetic responses to boron deficiency in Brassica napus: a review. Soil Sci Plant Nutr 60:304–313

    Article  CAS  Google Scholar 

  • Zhou T, Hua YP, Zhang BC, Zhang XQ, Zhou YH, Shi L, Xu FS (2017) Low-boron tolerance strategies involving pectin-mediated cell wall mechanical properties in Brassica napus Plant Cell Physiol 58:1991–2005

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by China Agriculture Research System (CARS-170204) and the Science and Technology Program of Guangzhou, China (202102020229).

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Authors and Affiliations

  1. Engineering Research Center of Agricultural Microbiology Technology, Ministry of Education, Heilongjiang University, Harbin, 150500, China

    Xin Song, Baiquan Song, Jialu Huo & Xiangling Wang

  2. Heilongjiang Provincial Key Laboratory of Ecological Restoration and Resource Utilization for Cold Region, School of Life Sciences, Heilongjiang University, Harbin, 150080, China

    Xin Song, Baiquan Song, Jialu Huo & Xiangling Wang

  3. College of Resources and Environment, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China

    Muhammad Riaz & Shaopeng Zhao

  4. Heilongjiang Academy of Agricultural Sciences, Safety and Quality Institute of Agricultural Products, Harbin, 150086, China

    Wengong Huang

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  1. Xin Song
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  2. Baiquan Song
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  3. Jialu Huo
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  4. Muhammad Riaz
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  5. Xiangling Wang
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Contributions

Xin Song: writing—original draft preparation and performing the experiments. Baiquan Song: designing the experiments. Xin Song, Baiquan Song, Jialu Huo, and Muhammad Riaz: analyzing the data. Baiquan Song, Muhammad Riaz, Xiangling, Wang, Wengong Huang, and Shaopeng Zhao: writing—reviewing.

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Correspondence to Baiquan Song.

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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 22, 4217–4227 (2022). https://doi.org/10.1007/s42729-022-01020-6

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