Regulation of Monocot and Dicot Plant Development with Constitutively Active Alleles of Phytochrome B

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Regulation of Monocot and Dicot Plant Development with Constitutively Active Alleles of Phytochrome B UC Davis UC Davis Previously Published Works Title Regulation of monocot and dicot plant development with constitutively active alleles of phytochrome B. Permalink https://escholarship.org/uc/item/2p11v031 Journal Plant direct, 4(4) ISSN 2475-4455 Authors Hu, Wei Figueroa-Balderas, Rosa Chi-Ham, Cecilia et al. Publication Date 2020-04-27 DOI 10.1002/pld3.210 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Received: 3 December 2019 | Revised: 3 February 2020 | Accepted: 25 February 2020 DOI: 10.1002/pld3.210 ORIGINAL RESEARCH Regulation of monocot and dicot plant development with constitutively active alleles of phytochrome B Wei Hu1 | Rosa Figueroa-Balderas2,3 | Cecilia Chi-Ham2 | J. Clark Lagarias1 1Department of Molecular and Cellular Biology, University of California, Davis, CA, Abstract USA The constitutively active missense allele of Arabidopsis phytochrome B, AtPHYBY276H 2 Public Intellectual Property Resource for or AtYHB, encodes a polypeptide that adopts a light-insensitive, physiologically active Agriculture (PIPRA), University of California, Davis, CA, USA conformation capable of sustaining photomorphogenesis in darkness. Here, we show 3Department of Viticulture and Enology, that the orthologous OsYHB allele of rice phytochrome B (OsPHYBY283H) also encodes University of California, Davis, CA, USA a dominant “constitutively active” photoreceptor through comparative phenotypic Correspondence analyses of AtYHB and OsYHB transgenic lines of four eudicot species, Arabidopsis Wei Hu, Department of Molecular and Cellular Biology, University of California, thaliana, Nicotiana tabacum (tobacco), Nicotiana sylvestris and Solanum lycopersicum Davis, CA 95616, USA. cv. MicroTom (tomato), and of two monocot species, Oryza sativa ssp. japonica and Email: [email protected] Brachypodium distachyon. Reciprocal transformation experiments show that the gain- Funding information of-function constitutive photomorphogenic (cop) phenotypes by YHB expression are This work was supported by grants to J.C.L. from the National Institutes of Health stronger in host plants within the same class than across classes. Our studies also (NIGMS GM068552), the National Science reveal additional YHB-dependent traits in adult plants, which include extreme shade Foundation (IOS-1239577), and the USDA National Institute of Food and Agriculture tolerance, both early and late flowering behaviors, delayed leaf senescence, reduced (CA-D*-MCB-4126-H). The contents of this tillering, and even viviparous seed germination. However, the strength of these gain- report are solely the responsibility of the authors and do not necessarily represent the of-function phenotypes depends on the specific combination of YHB allele and spe- official views of the NIH, NSF, or USDA. cies/cultivar transformed. Flowering and tillering of OsYHB- and OsPHYB-expressing lines of rice Nipponbare and Kitaake cultivars were compared, also revealing differ- ences in YHB/PHYB allele versus genotype interaction on the phenotypic behavior of the two rice cultivars. In view of recent evidence that the regulatory activity of AtYHB is not only light insensitive but also temperature insensitive, selective YHB expression is expected to yield improved agronomic performance of both dicot and monocot crop plant species not possible with wild-type PHYB alleles. KEYWORDS flowering regulation, light signal transduction, photobiology, photoperiodism, phytochrome, shade avoidance This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2020 The Authors. Plant Direct published by American Society of Plant Biologists, Society for Experimental Biology and John Wiley & Sons Ltd. Plant Direct. 2020;4:1–19. wileyonlinelibrary.com/journal/pld3 | 1 2 | HU ET AL. 1 | INTRODUCTION can flower early in non-inductive photoperiods (Bagnall et al., 1995; Hajdu et al., 2015; Krall & Reed, 2000; Oka et al., 2004; Song et al., Plants possess an array of photoreceptors that mediate real-time 2015; Wallerstein, Wallerstein, Libman, Machnic, & Whitelam, 2002; light acclimation responses to optimize light capture and energy Wu, Zhang, Li, & Fu, 2011; Zhang, Stankey, & Vierstra, 2013), late resource allocation. Among the best studied of these sensors are in inductive and non-inductive photoperiods (Bagnall & King, 2001; the phytochromes, which mainly monitor red (R) and far-red (FR) Halliday, Thomas, & Whitelam, 1997; Hwang et al., 2014; Song et al., light fluences informing growth and developmental decisions that 2015), at the same time as WT (Endo, Nakamura, Araki, Mochizuki, primarily impact competition with neighboring plants (Ballare & & Nagatani, 2005; Palagyi et al., 2010; Schittenhelm, Menge- Pierik, 2017; Casal, 2013; de Wit, Galvao, & Fankhauser, 2016). Hartmann, & Oldenburg, 2004; Thiele, Herold, Lenk, Quail, & Gatz, Phytochromes sense visible light using a linear tetrapyrrole (bilin) 1999; Usami, Matsushita, Oka, Mochizuki, & Nagatani, 2007; Zheng, chromophore that is covalently linked to a conserved cysteine res- Yang, Jang, & Metzger, 2001), and even exhibit novel phenotypes idue in a multidomain apoprotein (Anders & Essen, 2015; Burgie & inconsistent with SAR suppression (Viczian, Klose, Adam, & Nagy, Vierstra, 2014; Rockwell, Su, & Lagarias, 2006). Plant PHY apopro- 2017). teins comprise an N-terminal photosensory “light input” module con- These observations underscore our incomplete understanding sisting of highly conserved PAS, GAF, and PHY domains, and a more of phyB's regulatory roles in plants and also challenge the tacit as- diverged C-terminal regulatory “signal output” module with two PAS sumption from model systems that these roles will be conserved in domains and a histidine kinase-related domain (HKRD) (Nagatani, all plant species. It is well established that phyB signaling requires 2010). Photoisomerization of the C15 double bond of the bilin chro- formation of stable and transient complexes with transcription mophore initiates the reversible interconversion between the inac- regulators, components of the proteasome, and factors that affect tive R-absorbing Pr form and the active FR-absorbing Pfr form of the circadian clock (Bae & Choi, 2008; Viczian et al., 2017; Wang & holophytochromes (phys), triggering structural changes throughout Wang, 2014). PhyB also can form heterodimers with other phys, that the polypeptide that are recognized by downstream signaling effec- is, with phyC-E in Arabidopsis (Clack et al., 2009; Sharrock & Clack, tors (Bae & Choi, 2008; von Horsten et al., 2016; Pham, Kathare, & 2004). Hence, the relative abundances of phyB homodimers and Huq, 2018). these heterodimeric species change when phyB levels are altered. As master regulators of plant growth and development, phys The regulatory behavior is even more complicated when phyB from influence seed germination, vegetative growth, photoperiodic flow- one plant species is expressed in another, since the affinity of the ering, storage organ development, photosynthesis, senescence, introduced phyB with endogenous phys and/or with other down- shade avoidance responses (SARs), and phase/amplitude of the stream signaling components cannot be assumed to be the same as circadian clock (Demotes-Mainard et al., 2016; Franklin & Quail, that occurring in the host. While this complexity accounts for the 2010). For this reason, phys have been a target of crop improve- difficulty to predict the phenotypic consequences of phyB expres- ment efforts for over three decades (Keller, Shanklin, Vierstra, & sion, it also implicates the potential of tailored phyB expression to Hershey, 1989; Smith, 1992; Smith, Casal, & Jackson, 1990). Three modify selective aspects of light-mediated development of crop major PHY lineages are present in flowering plant genomes, PHYA, plants without affecting others. PHYB, and PHYC, with gene expansion and/or loss having occurred Here, we exploited YHB alleles of rice (Oryza sativum) and in some eudicot species (Alba, Kelmenson, Cordonnier-Pratt, & Arabidopsis PHYB, the latter of which has been proven to be Pratt, 2000; Clack, Mathews, & Sharrock, 1994; Karve et al., 2012; constitutively active regardless of the light conditions (Hu, Su, & Mathews, 2010; Sheehan, Farmer, & Brutnell, 2004; Takano et al., Lagarias, 2009; Su & Lagarias, 2007). We reasoned that, as domi- 2005). Transgenic phytochrome-based crop improvement efforts nant alleles, YHBs could be used to suppress SARs in any plant cul- have predominantly exploited PHYA overexpression because, unlike tivar to mitigate deleterious consequences on crop performance phyB, phyA remains active in FR-enriched shade light (Ganesan, Lee, at high planting densities. Our studies examined the phenotypic Kim, & Song, 2017). SARs that include rapid internode elongation, consequences of heterologous expression of AtYHB in three eu- enhanced apical dominance, reduced photosynthesis efficiency, dicot species, tomato (Solanum lycopersicum) and two Nicotiana premature flowering and increased susceptibility to pathogen in- species (N. tabacum and N. sylvestris), and in the monocot species fection, reduce crop yields as plant density is increased (Carriedo, rice. Homologous OsPHYB- and OsYHB-expressing rice lines were Maloof, & Brady, 2016). Triggered when phyB is inactivated by FR constructed for comprehensive
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