Tree architecture: A strigolactone-deficient mutant reveals a connection between branching order and auxin gradient along the tree stem

. 2023 Nov 28 ; 120 (48) : e2308587120. [epub] 20231122

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37991945

Due to their long lifespan, trees and bushes develop higher order of branches in a perennial manner. In contrast to a tall tree, with a clearly defined main stem and branching order, a bush is shorter and has a less apparent main stem and branching pattern. To address the developmental basis of these two forms, we studied several naturally occurring architectural variants in silver birch (Betula pendula). Using a candidate gene approach, we identified a bushy kanttarelli variant with a loss-of-function mutation in the BpMAX1 gene required for strigolactone (SL) biosynthesis. While kanttarelli is shorter than the wild type (WT), it has the same number of primary branches, whereas the number of secondary branches is increased, contributing to its bush-like phenotype. To confirm that the identified mutation was responsible for the phenotype, we phenocopied kanttarelli in transgenic BpMAX1::RNAi birch lines. SL profiling confirmed that both kanttarelli and the transgenic lines produced very limited amounts of SL. Interestingly, the auxin (IAA) distribution along the main stem differed between WT and BpMAX1::RNAi. In the WT, the auxin concentration formed a gradient, being higher in the uppermost internodes and decreasing toward the basal part of the stem, whereas in the transgenic line, this gradient was not observed. Through modeling, we showed that the different IAA distribution patterns may result from the difference in the number of higher-order branches and plant height. Future studies will determine whether the IAA gradient itself regulates aspects of plant architecture.

Biosciences Division Oak Ridge National Laboratory Oak Ridge TN 37830

Center for Bioscience Research and Education Utsunomiya University Utsunomiya 321 8505 Japan

Center of Plant Systems Biology and Biotechnology 4000 Plovdiv Bulgaria

Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University and Institute of Experimental Botany of the Academy of Sciences of the Czech Republic Olomouc 78371 Czech Republic

Department of Forest Genetics and Plant Physiology Umeå Plant Science Centre Swedish University of Agricultural Sciences 90183 Umeå Sweden

Institute of Biotechnology Helsinki Institute of Life Science University of Helsinki Helsinki 00014 Finland

Key Laboratory of Horticultural Plant Biology of Ministry of Education College of Horticulture and Forestry Sciences Huazhong Agricultural University Wuhan 430070 China

Laboratoire de Reproduction et Développement des Plantes École Normale Supérieure de Lyon Institut National de la Recherche Agronomique Lyon 69342 France

Laboratory of Growth Regulators Institute of Experimental Botany of the Czech Academy of Sciences Faculty of Science of Palacký University Olomouc CZ 78371 Czech Republic

Mathematics and Computer Science Adam Mickiewicz University Poznań 61 614 Poland

Mathematics Tampere University Tampere 33720 Finland

Max Planck Institute of Molecular Plant Physiology Potsdam Golm 14476 Germany

Molecular and Integrative Biosciences Research Program Faculty of Biological and Environmental Sciences and Viikki Plant Science Centre University of Helsinki Helsinki 00014 Finland

National Plant Phenotyping Infrastructure Helsinki Institute of Life Science University of Helsinki Biocenter Finland Helsinki 00014 Finland

Organismal and Evolutionary Biology Research Program Faculty of Biological and Environmental Sciences Viikki Plant Science Centre University of Helsinki Helsinki 00014 Finland

Production Systems Natural Resources Institute Finland Helsinki 00790 Finland

Sainsbury Laboratory University of Cambridge Cambridge CB2 1LR United Kingdom

School of Biological Sciences Nanyang Technological University Singapore 637551 Singapore

Zobrazit více v PubMed

Petit R. J., Hampe A., Some evolutionary consequences of being a tree. Annu. Rev. Ecol. Evol. Syst. 37, 187–214 (2006).

Leverenz J. W., Photosynthesis and transpiration in large forest-grown Douglas-fir: Interactions with apical control. Can. J. Bot. 59, 2568–2576 (1981).

Suzuki A. A., Shoot growth patterns in saplings of Cleyera japonica in relation to light and architectural position. Tree Physiol. 23, 67–71 (2003). PubMed

Maillette L., Structural dynamics of silver Birch. I. The fates of buds. J. Appl. Ecol. 19, 203–218 (1982).

Suzuki A. A., Suzuki M., Why do lower order branches show greater shoot growth than higher order branches? Considering space availability as a factor affecting shoot growth. Trees 23, 69–77 (2009).

Galinat W. C., The phytomer in relation to floral homologies in the American Maydeae. Bot. Mus. Leafl., Harv. Univ. 19, 1–32 (1959).

Salojarvi J., et al. , Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat. Genet. 49, 904 (2017). PubMed

Alonso-Serra J., et al. , Tissue-specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol. 222, 1816–1831 (2019). PubMed

Longman K. A., Wareing P. F., Early induction of flowering in birch seedlings. Nature 184, 2037–2038 (1959).

Keinonen-Mettälä K., Pappinen A., von Weissenberg K., Comparisons of the efficiency of some promoters in silver birch (Betula pendula). Plant Cell Rep. 17, 356–361 (1998). PubMed

Ward S. P., Salmon J., Hanley S. J., Karp A., Leyser O., Using Arabidopsis to study shoot branching in biomass willow. Plant Physiol. 162, 800–811 (2013). PubMed PMC

Salmon J., Ward S. P., Hanley S. J., Leyser O., Karp A., Functional screening of willow alleles in Arabidopsis combined with QTL mapping in willow (Salix) identifies SxMAX4 as a coppicing response gene. Plant Biotechnol. J. 12, 480–491 (2014). PubMed PMC

Xie X., Structural diversity of strigolactones and their distribution in the plant kingdom. J. Pestic. Sci. 41, 175–180 (2016). PubMed PMC

Yoneyama K., et al. , Which are the major players, canonical or non-canonical strigolactones? J. Exp. Bot. 69, 2231–2239 (2018). PubMed

Yoneyama K., Kisugi T., Xie X., Yoneyama K., “Chemistry of strigolactones: Why and how do plants produce so many strigolactones?” in Molecular Microbial Ecology of the Rhizosphere (Wiley, 2013), pp. 373–379, 10.1002/9781118297674.ch34. DOI

Akiyama K., Matsuzaki K., Hayashi H., Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005). PubMed

Akiyama K., Hayashi H., Strigolactones: Chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann. Bot. 97, 925–931 (2006). PubMed PMC

Matusova R., et al. , The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 139, 920–934 (2005). PubMed PMC

Al-Babili S., Bouwmeester H. J., Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol. 66, 161–186 (2015). PubMed

Jia K.-P., Baz L., Al-Babili S., From carotenoids to strigolactones. J. Exp. Bot. 69, 2189–2204 (2017). PubMed

Sorefan K., et al. , MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes. Dev. 17, 1469–1474 (2003). PubMed PMC

Booker J., et al. , MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 14, 1232–1238 (2004). PubMed

Booker J., et al. , MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev. Cell 8, 443–449 (2005). PubMed

Domagalska M. A., Leyser O., Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12, 211–221 (2011). PubMed

Mason M. G., Ross J. J., Babst B. A., Wienclaw B. N., Beveridge C. A., Sugar demand, not auxin, is the initial regulator of apical dominance. Proc. Natl. Acad. Sci. U.S.A. 111, 6092–6097 (2014). PubMed PMC

Bertheloot J., et al. , Sugar availability suppresses the auxin-induced strigolactone pathway to promote bud outgrowth. New Phytol. 225, 866–879 (2020). PubMed

Stirnberg P., Furner I. J., Ottoline Leyser H. M., MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 50, 80–94 (2007). PubMed

Shen H., Luong P., Huq E., The F-Box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 145, 1471–1483 (2007). PubMed PMC

Brewer P. B., et al. , LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 113, 6301–6306 (2016). PubMed PMC

Gomez-Roldan V., et al. , Strigolactone inhibition of shoot branching. Nature 455, 189–U122 (2008). PubMed

Stirnberg P., van de Sande K., Leyser H. M. O., MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129, 1131–1141 (2002). PubMed

Umehara M., et al. , Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195–200 (2008). PubMed

Bennett T., et al. , Strigolactone regulates shoot development through a core signalling pathway. Biol. Open 5, 1806–1820 (2016). PubMed PMC

Sang D., et al. , Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 111, 11199–11204 (2014). PubMed PMC

Calders K., et al. , Terrestrial laser scanning in forest ecology: Expanding the horizon. Remote Sens. Environ. 251, 112102 (2020).

Raumonen P., Brede B., Lau A., Bartholomeus H., “A shortest path based tree isolation method for UAV LiDAR data” in 2021 IEEE International Geoscience and Remote Sensing Symposium (IGARSS) (2021), pp. 724–727.

Raumonen P., et al. , Fast automatic precision tree models from terrestrial laser scanner data. Remote Sens. 5, 491–520 (2013).

NaPPI (National Plant Phenotyping Infrastructure), https://www.helsinki.fi/en/infrastructures/national-plant-phenotyping. Accessed 3 February 2023.

Snow R., Experiments on growth inhibition. Part II—New phenomena of inhibition. Proc. R. Soc. Lond. Ser. B, Biol. Sci. 108, 305–316 (1931).

Morris D. A., Transport of exogenous auxin in 2-branched dwarf pea-seedlings (Pisum sativum L.)—Some implications for polarity and apical dominance. Planta 136, 91–96 (1977). PubMed

Thimann K. V., Skoog F., Studies on the growth hormone of plants: III. The inhibiting action of the growth substance on bud development. Proc. Natl. Acad. Sci. U.S.A. 19, 714–716 (1933). PubMed PMC

Bennett T., et al. , The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16, 553–563 (2006). PubMed

Muhr M., Prufer N., Paulat M., Teichmann T., Knockdown of strigolactone biosynthesis genes in Populus affects BRANCHED1 expression and shoot architecture. New Phytol. 212, 613–626 (2016). PubMed

Brewer P. B., Dun E. A., Ferguson B. J., Rameau C., Beveridge C. A., Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol. 150, 482–493 (2009). PubMed PMC

Shinohara N., Taylor C., Leyser O., Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 11, e1001474 (2013). PubMed PMC

Fichtner F., et al. , Regulation of shoot branching in Arabidopsis by trehalose 6-phosphate. New Phytol. 229, 2135–2151 (2021). PubMed

Prusinkiewicz P., et al. , Control of bud activation by an auxin transport switch. Proc. Natl. Acad. Sci. U.S.A. 106, 17431–17436 (2009). PubMed PMC

Turnbull C. G. N., Booker J. P., Leyser H. M. O., Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255–262 (2002). PubMed

Beveridge C. A., Ross J. J., Murfet I. C., Branching mutant rms-2 in Pisum sativum (Grafting studies and endogenous indole-3-acetic acid levels). Plant Physiol. 104, 953–959 (1994). PubMed PMC

Foo E., Turnbull C. G. N., Beveridge C. A., Long-distance signaling and the control of branching in therms1 mutant of pea. Plant Physiol. 126, 203–209 (2001). PubMed PMC

Morris S. E., Turnbull C. G. N., Murfet I. C., Beveridge C. A., Mutational analysis of branching in pea. Evidence ThatRms1 and Rms5 regulate the same novel signal. Plant Physiol. 126, 1205–1213 (2001). PubMed PMC

Napoli C., Highly branched phenotype of the Petunia dad1-1 mutant is reversed by grafting. Plant Physiol. 111, 27–37 (1996). PubMed PMC

Kohlen W., et al. , Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol. 155, 974–987 (2011). PubMed PMC

von Arx G., Arzac A., Olano J. M., Fonti P., Assessing conifer ray parenchyma for ecological studies: Pitfalls and guidelines. Front. Plant Sci. 6, 1016 (2015). PubMed PMC

Su C., Zenodo badge. Zenodo. https://zenodo.org/badge/633505761.svg. Deposited 26 July 2023.

Su C., Kokosza A., ChangBio/kanttarelli. Github. https://github.com/ChangBio/kanttarelli.git. Deposited 26 July 2023.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...