Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-26T22:29:58.442Z Has data issue: false hasContentIssue false
  • English
  • Français

Dynamics of the contents and distribution of ABA, auxins and aquaporins in developing caryopses of an ABA-deficient barley mutant and its parental cultivar

Published online by Cambridge University Press:  11 December 2019

Oksana A. Seldimirova Open the ORCID record for Oksana A. Seldimirova [Opens in a new window] ,
Guzel R. Kudoyarova Open the ORCID record for Guzel R. Kudoyarova [Opens in a new window] ,
Maki Katsuhara ,
Ilshat R. Galin ,
Denis Yu. Zaitsev ,
Natalia N. Kruglova Open the ORCID record for Natalia N. Kruglova [Opens in a new window] ,
Dmitry S. Veselov  and
Stanislav Yu. Veselov
Oksana A. Seldimirova*
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Guzel R. Kudoyarova
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Maki Katsuhara
Affiliation:
Okayama University, Institute of Plant Science and Resources, Kurashiki, Okayama710-0046, Japan
Ilshat R. Galin
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Denis Yu. Zaitsev
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Natalia N. Kruglova
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Dmitry S. Veselov
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia
Stanislav Yu. Veselov
Affiliation:
Ufa Institute of Biology, Ufa Federal Research Centre, Russian Academy of Sciences, pr. Oktyabrya 69, Ufa450054, Russia Department of Biochemistry and Biotechnology, Faculty of Biology, Bashkir State University, Zaki Validi Street 32, Ufa450076, Russia
*
Author for correspondence: Oksana A. Seldimirova, Email: o_seldimirova@mail.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

Dynamics of abscisic acid (ABA) and indole-3-acetic acid (IAA) contents were followed in developing barley caryopses of the ABA-deficient mutant AZ34 and its parental cultivar Steptoe. Distribution of these hormones and HvPIP2 aquaporins (AQPs) was studied with the help of immunohistochemical methods in the roots and coleorhiza of developing embryos. In Steptoe, maturation of the caryopsis was accompanied by vast accumulation of ABA, while this hormone accumulated more slowly in the caryopsis of AZ34 and its content was lower than in Steptoe. Accumulation of ABA was accompanied by a decline in IAA level in the developing caryopsis, the process being delayed in AZ34 in accordance with the slower accumulation of ABA. ABA accumulated to high levels in the coleorhiza cells of Steptoe, while the effect was absent in AZ34. The high level of ABA was likely to be important for maintaining the barrier function of the coleorhiza, preventing germination of seminal roots and enabling seed dormancy, while the absence of ABA accumulation in coleorhiza of AZ34 may be responsible for the initiation of root germination inside the caryopsis. The abundance of HvPIP2 AQPs in the seminal roots was higher at the beginning of maturation of Steptoe caryopsis and declined afterwards, while the levels of APQs increased later in AZ34 in accordance with the delay in ABA accumulation. These results suggest the importance of ABA accumulation in coleorhiza for preventing precocious growth of seminal roots, and suggest regulation of IAA and aquaporin levels by this hormone during maturation of embryos.

Keywords

abscisic acidaquaporinauxinbarleycaryopsis developmentembryo formation
Type
Research Paper
Information
Seed Science Research , Volume 29 , Issue 4 , December 2019 , pp. 261 - 269
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barrero, JM, Talbot, MJ, White, RG, Jacobsen, JV and Gubler, F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiology 150, 1006–1021.CrossRefGoogle ScholarPubMed
Benková, E, Michniewicz, M, Sauer, M, Teichmann, T, Seifertová, D, Jürgens, G and Friml, J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602.CrossRefGoogle ScholarPubMed
Cheng, ZJ, Zhao, XY, Shao, XX, Wang, F, Zhou, C, Liu, YG, Zhang, Y and Zhang, XS (2014) Abscisic acid regulates early seed development in Arabidopsis by ABI5-mediated transcription of SHORT HYPOCOTYL UNDER BLUE. Plant Cell 26, 1053–1068.CrossRefGoogle Scholar
Ciavatta, VT, Morillon, R, Pullman, GS, Chrispeels, MJ and Cairney, J (2001) An aquaglyceroporin is abundantly expressed early in the development of the suspensor and the embryo proper of loblolly pine. Plant Physiology 127, 1556–1567.CrossRefGoogle ScholarPubMed
Doll, NM, Depege-Fargeix, N, Rogowsky, PM and Widiez, T (2017) Signaling in early maize kernel development. Molecular Plant 10, 375–388.CrossRefGoogle ScholarPubMed
Forestan, C, Meda, S and Varotto, S (2010) ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiology 152, 1373–1390.CrossRefGoogle ScholarPubMed
Friml, J, Vieten, A, Sauer, M, Weijers, D, Schwarz, H, Hamann, T, Offringa, R and Jürgens, G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153.CrossRefGoogle ScholarPubMed
Fu, J, Yu, H, Li, X, Xiao, J and Wang, S (2011) Rice GH3 gene family: regulators of growth and development. Plant Signaling and Behavior 6, 570–574.CrossRefGoogle ScholarPubMed
Hess, JR, Carman, JG and Banowetz, GM (2002) Hormones in wheat kernels during embryony. Plant Physiology 159, 379–386.CrossRefGoogle Scholar
Horie, T, Kaneko, T, Sugimoto, G, Sasano, S, Panda, SK, Shibasaka, M and Katsuhara, M (2011) Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant and Cell Physiology 52, 663–675.CrossRefGoogle ScholarPubMed
Kaldenhoff, R, Ribas-Carbo, M, Sans, JF, Lovisolo, C, Heckwolf, M and Uehlein, N (2008) Aquaporins and plant water balance. Plant, Cell & Environment 31, 658–666.CrossRefGoogle ScholarPubMed
Kudoyarova, G, Veselova, S, Hartung, W, Farhutdinov, R, Veselov, D and Sharipova, G (2011) Involvement of root ABA and hydraulic conductivity in the control of water relations in wheat plants exposed to increased evaporation demand. Planta 233, 87–94.CrossRefGoogle Scholar
Kucera, B, Cohn, MA and Leubner-Metzger, G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.CrossRefGoogle Scholar
Li, SW, Leng, Y, Feng, L and Zeng, XY (2014) Involvement of abscisic acid in regulating antioxidative defense systems and IAA-oxidase activity and improving adventitious rooting in mung bean [Vigna radiata (L.) Wilczek] seedlings under cadmium stress. Environmental Science and Pollution Research 21, 525–537.CrossRefGoogle ScholarPubMed
Lin, W, Peng, Y, Li, G, Arora, R, Tang, Z, Su, W and Cai, W (2007) Isolation and functional characterization of PgTIP1, a hormone-autotrophic cells-specific tonoplast aquaporin in ginseng. Journal of Experimental Botany 58, 947–956.CrossRefGoogle ScholarPubMed
Liu, B, Liu, X, Wang, C, Jin, J and Herbert, SJ (2010) Endogenous hormones in seed, leaf, and pod wall and their relationship to seed filling in soybeans. Crop and Pasture Science 61, 103–110.CrossRefGoogle Scholar
Liu, X, Zhang, H, Zhao, Y, Feng, Z, Li, Q, Yang, HQ, Luan, S, Li, J and He, ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy Sciences of the USA 110, 15485–15490.CrossRefGoogle ScholarPubMed
Locascio, A, Roig-Villanova, I, Bernardi, J and Varotto, S (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Frontiers in Plant Sciences 5, 412.Google ScholarPubMed
Lur, HS and Setter, TL (1993) Role of auxin in maize endosperm development (timing of nuclear DNA endoreduplication, zein expression, and cytokinin). Plant Physiology 103, 273–280.CrossRefGoogle Scholar
Luxová, M (1986) The seminal root primordia in barley and the participation of their non-meristematic cells in root construction. Biologia Plantarum 28, 161–167.CrossRefGoogle Scholar
Lynn, JA (1965) Rapid toluidine blue staining of Epon-embedded and mounted «adjacent» sections. American Journal of Clinical Pathology. 44, 57–58. doi: 10.1093/jxb/erv244CrossRefGoogle ScholarPubMed
Mao, Z and Sun, W (2015) Arabidopsis seed-specific vacuolar aquaporins are involved in maintaining seed longevity under the control of ABSCISIC ACID INSENSITIVE 3. Journal of Experimental Botany 66, 4781–7894.CrossRefGoogle ScholarPubMed
Obroucheva, NV (2013) Aquaporins in seeds. Seed Science Research 23, 213–216.CrossRefGoogle Scholar
Péret, B, Li, G, Zhao, J, Band, LR, Voß, U, Postaire, O, Luu, DT, Da Ines, O, Casimiro, I, Lucas, M, Wells, DM, Lazzerini, L, Nacry, P, King, JR, Jensen, OE, Schäffner, AR, Maurel, C and Bennett, MJ (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology 14, 991–998.CrossRefGoogle ScholarPubMed
Schuurmans, JAMJ, van Dongen, JT, Rutjens, BPS, Boonman, A, Pieterse, CMJ and Borstlap, AC (2003) Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP and NIP subfamilies. Plant Molecular Biology 53, 655–667.CrossRefGoogle ScholarPubMed
Seldimirova, OA, Kudoyarova, GR, Kruglova, NN, Zaytsev, D, Yu, S and Veselev, S (2016) Changes in distribution of cytokinins and auxins in cells during callus induction and organogenesis in vitro in immature embryo culture of wheat. In Vitro Cellular and Developmental Biology – Plant 52, 251–264.CrossRefGoogle Scholar
Seo, PJ, Xiang, F, Qiao, M, Park, JY, Lee, YN, Kim, SG, Lee, YH, Park, WJ and Park, CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiology 151, 275–289.CrossRefGoogle ScholarPubMed
Sharipova, G, Veselov, D, Kudoyarova, G, Fricke, W, Dodd, I, Katsuhara, M, Furuichi, T, Ivanov, I and Veselov, S (2016) Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA deficient barley mutant Az34. Annals of Botany 118, 777–785.CrossRefGoogle ScholarPubMed
Shiota, H, Sudoh, T and Tanaka, I (2006) Expression analysis of genes encoding plasma membrane aquaporins during seed and fruit development in tomato. Plant Science 171, 277–285.CrossRefGoogle Scholar
Shu, K, Liu, X-D, Xie, Q and He, Z-H (2016). Two faces of one seed: hormonal regulation of dormancy and germination. Molecular Plant 9, 34–45.CrossRefGoogle ScholarPubMed
Son, S, Chitnis, VR, Liu, A, Gao, F, Nguyen, T-N and Ayele, BT (2016). Abscisic acid metabolic genes of wheat (Triticum aestivum L.): identification and insights into their functionality in seed dormancy and dehydration tolerance. Planta 244, 429–447.CrossRefGoogle ScholarPubMed
Tuan, PA, Kumar, R, Rehal, PK, Toora, PK and Ayele, BT (2018) Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Frontiers Plant Science 9, art. 688.CrossRefGoogle ScholarPubMed
Ulferts, S, Delventhal, R, Splivallo, R, Karlovsky, P and Schaffrath, U (2015) Abscisic acid negatively interferes with basal defence of barley against Magnaporthe oryzae. BMC Plant Biology 15, 7. doi: 10.1186/s12870-014-0409-xCrossRefGoogle ScholarPubMed
Veselov, SU, Kudoyarova, GR, Egutkin, NL, Gyuli-Zade, VG, Mustafina, AR and Kof, EK (1992) Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole 3-acetic acid. Physiologia Plantarum 86, 93–96.CrossRefGoogle Scholar
Veselov, DS, Sharipova, GV, Veselov, S, Yu, S, Dodd, IC, Ivanov, I and Kudoyarova, GR (2018) Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand. Functional Plant Biology 45, 143–149.CrossRefGoogle Scholar
Vysotskaya, LB, Arkhipova, TN, Kudoyarova, GR and Veselov, SY (2018) Dependence of growth inhibiting action of increased planting density on capacity of lettuce plants to synthesize ABA. Journal of Plant Physiology 220, 69–73.CrossRefGoogle ScholarPubMed
Walker-Simmons, M, Kudrna, DA and Warner, RL (1989) Reduced accumulation of aba during water stress in a molybdenum cofactor mutant of barley. Plant Physiology 90, 728–33.CrossRefGoogle Scholar
Werner, M, Uehlein, N, Proksch, P and Kaldenhoff, R (2001) Characterization of two tomato quaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta reflexa. Planta 213, 550–555.CrossRefGoogle Scholar
Yang, J, Zhang, J, Wang, Z and Zhu, Q (2003) Hormones in the grains in relation to sink strength and postanthesis development of spikelets in rice. Plant Growth Regulation 41, 185–195.CrossRefGoogle Scholar
Zhou, Y, Setz, N, Niemietz, C, Qu, H, Offler, CE, Tyerman, SD and Patrick, JW (2007) Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant Cell and Environment 30, 1566–1577.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Seldimirova et al. supplementary material

Seldimirova et al. supplementary material 1
Download Seldimirova et al. supplementary material(Image)
Image 1.8 MB
Supplementary material: Image

Seldimirova et al. supplementary material

Seldimirova et al. supplementary material 2

Download Seldimirova et al. supplementary material(Image)
Image 1.8 MB
Supplementary material: File

Seldimirova et al. supplementary material

Seldimirova et al. supplementary material 3

Download Seldimirova et al. supplementary material(File)
File 41 KB