About PBA

Boron functions in plants

Schematic of boric acid and phenylboronic acid uptake
© Michaela Matthes

Figure 1 Schematic of boric acid and phenylboronic acid uptake into the plant cell and their hypothesized crosslinking/binding to Rhamnogalacturonan-II (RG-II) in the cell wall. Taken from (Matthes et al., 2020).

Plants take up boron in the form of boric acid (Fig. 1) (reviewed in Matthes et al., 2020). All known molecular functions of boron are related to its ability to form reversible links with cis-diol groups, which are for example present in sugar molecules (Bolaños et al., 2004). So far, boron has only been shown to bind to and to crosslink the pectic subunit Rhamnogalacturonan-II (RG-II) in the primary cell wall (Kobayashi et al., 1996; Matoh et al., 1996; O’Neill et al., 1996). The cross linking of RG-II by boron contributes to the stability of the primary cell wall (O’Neill et al., 2001), yet cell wall defects are not sufficient to explain all boron deficiency-induced developmental defects. Some of the open questions in boron research today are whether boron can also bind or crosslink other molecules, and whether there are cell wall independent functions of boron. Additional binding partners of boron have been proposed (Wimmer et al., 2009; Voxeur and Fry, 2014) and reported cross-talks between boron and the phytohormones auxin, cytokinin, and ethylene (Blevins and Lukaszewski, 1998; Bolaños et al., 2004; Abreu et al., 2014; Camacho-Cristóbal et al., 2015; Li et al., 2015; Matthes and Torres-Ruiz, 2016; Gómez-soto et al., 2019) are promising targets for the identification of cell wall independent boron functions.

Why can Phenylboronic acid (PBA) be used to induce boron deficiency?

Similar to boric acid, chemical analogs like phenylboronic acid (PBA) can form esters with cis-diol groups. Unlike boric acid, PBA cannot crosslink two molecules (Fig. 1). Therefore, PBA is assumed to induce boron deficiency symptoms through competitively inhibiting boron crosslinking in the cell wall (Bassil et al., 2004) (Fig. 1) and offers a tool to address some of the open questions in boron research.

Root defects induced by PBA

Effects of PBA on maize root development.
© Michaela Matthes

Figure 2 Effects of PBA on maize root development. A) Primary root of a five-day-old maize seedling germinated in H2O. B) Histology of the primary root tip of a five-day-old maize seedling germinated in H2O. C) Primary root of a five-day-old maize seedling germinated in 5 mM PBA. D) Histology of the primary root tip of a five-day-old maize seedling germinated in 5 mM PBA. Scale bars in A,C: 2 cm, in B,D: 200 µm.

Maize kernels that are germinated in PBA develop into seedlings with shorter primary roots and reduced lateral root density compared to kernels that are germinated in H2O (Housh et al., 2020) (Fig. 2). PBA-induced maize root defects are similar to reported defects of root development under boron deficiency, like the reduction of root length, browning of the tissue, and swelling of the root tip (Dell and Huang, 1997) (Fig. 2). In addition, germination of maize kernels in PBA and boric acid leads to partial rescue of the PBA induced primary root length defects, supporting that the PBA induced defects in maize are due to boron deficiency.

Questions addressed in this project

  • How specific is PBA in inducing boron deficiency?
    Approach: Molecular and cellular characterization of PBA induced defects in the primary root tip and in lateral roots
  • Are there cell wall independent functions of boron?
    Approach: Characterization of cross-talk between boron and phytohormones (auxin, cytokinin, ethylene)
  • What are the targets of PBA?
    Approach: Forward chemical screens using the 282 Goodman panel (Flint-Garcia et al., 2005) and an EMS-induced mutant library

References:

  • Abreu I, Poza L, Bonilla I, Bolaños L. 2014. Boron deficiency results in early repression of a cytokinin receptor gene and abnormal cell differentiation in the apical root meristem of Arabidopsis thaliana. Plant Physiology and Biochemistry 77, 117–121.
  • Bassil E, Hu H, Brown PH. 2004. Use of Phenylboronic Acids to Investigate Boron Function in Plants . Possible Role of Boron in Transvacuolar Cytoplasmic Strands and Cell-to-Wall Adhesion. Plant Physiology 136, 3383–3395.
  • Blevins D, Lukaszewski K. 1998. Boron in Plant Structure and Function. Annual Review of Plant Physiology and Plant Molecular Biology 49, 481–500.
  • Bolaños L, Lukaszewski K, Bonilla I, Blevins D. 2004. Why boron? Plant Physiology and Biochemistry 42, 907–912.
  • Camacho-Cristóbal JJ, Martín-Rejano EM, Herrera-Rodríguez MB, Navarro-Gochicoa MT, Rexach J, González-Fontes A. 2015. Boron deficiency inhibits root cell elongation via an ethylene/auxin/ROS-dependent pathway in Arabidopsis seedlings. Journal of Experimental Botany 66, 3831–3840.
  • Dell B, Huang L. 1997. Physiological response of plants to low boron. Plant and Soil 193, 103–120.
  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES. 2005. Maize association population: A high-resolution platform for quantitative trait locus dissection. Plant Journal 44, 1054–1064.
  • Gómez-soto D, Galván S, Rosales E, Bienert P, Abreu I, Bonilla I, Bolaños L. 2019. Insights into the role of phytohormones regulating pAtNIP5 ; 1 activity and boron transport in Arabidopsis thaliana. Plant Science 287, 110198.
  • Housh AB, Matthes MS, Gerheart A, Wilder SL, Kil K, Schueller M, Guthrie JM, Mcsteen P, Ferrieri R. 2020. Assessment of a 18 F-Phenylboronic Acid Radiotracer for Imaging Boron in Maize. International Journal of Molecular Sciences 21.
  • Kobayashi M, Matoh T, Azuma J. 1996. Two Chains of Rhamnogalacturonan II Are Cross-Linked by Borate-Diol Ester Bonds in Higher Plant Cell Walls. Plant Physiology 110, 1017–1020.
  • Li K, Kamiya T, Fujiwara T. 2015. Differential roles of PIN1 and PIN2 in Root Meristem Maintenance Under Low-B Conditions in Arabidopsis thaliana. Plant and Cell Physiology 56, 1205–1214.
  • Matoh T, Kawaguchi S, Kobayashi M. 1996. Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants. Plant and Cell Physiology 37, 636–640.
    Matthes MS, Robil JM, Mcsteen P. 2020. From element to development : the power of the essential micronutrient boron to shape morphological processes in plants. Journal of Experimental Botany 71, 1681–1693.
  • Matthes M, Torres-Ruiz RA. 2016. Boronic acid treatment phenocopies monopteros by affecting PIN1 membrane stability and polar auxin transport in Arabidopsis thaliana embryos. Development 143, 4053–4062.
  • O’Neill MA, Eberhard S, Albersheim P, Darvill AG. 2001. Requirement of Borate Cross-linking of Cell Wall Rhamnogalacturonan II for Arabidopsis Growth. Science (New York, N.Y.) 294, 846–849.
  • O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P, De P, Viala 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. The Journal of Biological Chemistry 271, 22923–22930.
  • Voxeur A, Fry SC. 2014. Glycosylinositol phosphorylceramides from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan II. Plant Journal 79, 139–149.
  • Wimmer MA, Lochnit G, Bassil E, Mhling KH, Goldbach HE. 2009. Membrane-associated, boron-interacting proteins isolated by boronate affinity chromatography. Plant and Cell Physiology 50, 1292–1304.