SPL16 and SPL23 mediate photoperiodic control of seasonal growth in Populus trees.
Populus
SPL transcription factors
bud set
growth cessation
miR156
phyB-PIF module
short photoperiod
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
20 Dec 2023
20 Dec 2023
Historique:
received:
19
10
2023
accepted:
12
11
2023
medline:
20
12
2023
pubmed:
20
12
2023
entrez:
20
12
2023
Statut:
aheadofprint
Résumé
Perennial trees in boreal and temperate regions undergo growth cessation and bud set under short photoperiods, which are regulated by phytochrome B (phyB) photoreceptors and PHYTOCHROME INTERACTING FACTOR 8 (PIF8) proteins. However, the direct signaling components downstream of the phyB-PIF8 module remain unclear. We found that short photoperiods suppressed the expression of miR156, while upregulated the expression of miR156-targeted SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE 16 (SPL16) and SPL23 in leaves and shoot apices of Populus trees. Accordingly, either overexpression of MIR156a/c or mutagenesis of SPL16/23 resulted in the attenuation of growth cessation and bud set under short days (SD), whereas overexpression of SPL16 and SPL23 conferred early growth cessation. We further showed that SPL16 and SPL23 directly suppressed FLOWERING LOCUS T2 (FT2) expression while promoted BRANCHED1 (BRC1.1 and BRC1.2) expression. Moreover, we revealed that PIF8.1/8.2, positive regulators of growth cessation, directly bound to promoters of MIR156a and MIR156c and inhibited their expression to modulate downstream pathways. Our results reveal a connection between the phyB-PIF8 module-mediated photoperiod perception and the miR156-SPL16/23-FT2/BRC1 regulatory cascades in SD-induced growth cessation. Our study provides insights into the rewiring of a conserved miR156-SPL module in the regulation of seasonal growth in Populus trees.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Chongqing Major Special Project for Promoting Forestry through Science and Technology
ID : 2D-2022-2
Organisme : National Key Research and Development Program of China
ID : 2022YFD1201600
Organisme : National Natural Science Foundation of China
ID : 32101483
Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
André D, Marcon A, Lee KC, Goretti D, Zhang B, Delhomme N, Schmid M, Nilsson O. 2022. FLOWERING LOCUS T paralogs control the annual growth cycle in Populus trees. Current Biology 32: 2988-2996.
Azeez A, Miskolczi P, Tylewicz S, Bhalerao RP. 2014. A tree ortholog of APETALA1 mediates photoperiodic control of seasonal growth. Current Biology 24: 717-724.
Azeez A, Zhao YC, Singh RK, Yordanov YS, Dash M, Miskolczi P, Stojkovič K, Strauss SH, Bhalerao RP, Busov VB. 2021. EARLY BUD-BREAK 1 and EARLY BUD-BREAK 3 control resumption of poplar growth after winter dormancy. Nature Communications 12: 1123.
Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040-1043.
Cerdán PD, Chory J. 2003. Regulation of flowering time by light quality. Nature 423: 881-885.
Chen S, Songkumarn P, Liu J, Wang GL. 2009. A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiology 150: 1111-1121.
Ding J, Nilsson O. 2016. Molecular regulation of phenology in trees-because the seasons they are a-changin. Current Opinion in Plant Biology 29: 73-79.
Ding J, Zhang B, Li Y, André D, Nilsson O. 2021. Phytochrome B and PHYTOCHROME INTERACTING FACTOR8 modulate seasonal growth in trees. New Phytologist 232: 2339-2352.
Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K. 2015. Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports 5: 12217.
Galvāo VC, Fiorucci AS, Trevisan M, Franco-Zorilla JM, Goyal A, Schmid-Siegert E, Solano R, Fankhauser C. 2019. PIF transcription factors link a neighbor threat cue to accelerated reproduction in Arabidopsis. Nature Communications 10: 4005.
Gou J, Tang C, Chen N, Wang H, Debnath S, Sun L, Flanagan A, Tang Y, Jiang Q, Allen RD et al. 2019. SPL7 and SPL8 represent a novel flowering regulation mechanism in switchgrass. New Phytologist 222: 1610-1623.
Howe GT, Bucciaglia PA, Hackett WP, Furnier GR, Cordonnier-Pratt MM, Gardner G. 1998. Evidence that the phytochrome gene family in black cottonwood has one PHYA locus and two PHYB loci but lacks members of the PHYC/F and PHYE subfamilies. Molecular Biology and Evolution 15: 160-175.
Hu J, Su H, Cao H, Wei H, Fu X, Jiang X, Song Q, He X, Xu C, Luo K. 2022. AUXIN RESPONSE FACTOR7 integrates gibberellin and auxin signaling via interactions between DELLA and AUX/IAA proteins to regulate cambial activity in poplar. Plant Cell 34: 2688-2707.
Ibáñez C, Kozarewa I, Johansson M, Ögren E, Rohde A, Eriksson ME. 2010. Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiology 153: 1823-1833.
Jefferson RA. 1987. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Molecular Biology Reporter 5: 387-405.
Jia Z, Gou J, Sun Y, Yuan L, Tang Q, Yang X, Pei Y, Luo K. 2010. Enhanced resistance to fungal pathogens in transgenic Populus tomentosa Carr. by overexpression of an nsLTP-like antimicrobial protein gene from motherwort (Leonurus japonicus). Tree Physiology 30: 1599-1605.
Johansson M, Takata N, Ibáñez C, Eriksson ME. 2022. Monitoring seasonal bud set, bud burst, and cold hardiness in Populus. Methods in Molecular Biology 2398: 215-226.
Jung JH, Ju Y, Seo PJ, Lee JH, Park CM. 2012. The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. The Plant Journal 69: 577-588.
Jung JH, Lee HJ, Ryu JY, Park CM. 2016. SPL3/4/5 integrate developmental aging and photoperiodic signals into the FT-FD module in Arabidopsis flowering. Molecular Plant 9: 1647-1659.
Karlberg A, Bako L, Bhalerao RP. 2011. Short day-mediated cessation of growth requires the downregulation of AINTEGUMENTALIKE1 transcription factor in hybrid aspen. PLoS Genetics 7: e1002361.
Karve AA, Jawdy SS, Gunter LE, Allen SM, Yang X, Tuskan GA, Wullschleger SD, Weston DJ. 2012. Initial characterization of shade avoidance response suggests functional diversity between Populus phytochrome B genes. New Phytologist 196: 726-737.
Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH. 2012. The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiology 159: 461-478.
Kozarewa I, Ibáñez C, Johansson M, Ögren E, Mozley D, Nylander E, Chono M, Moritz T, Eriksson ME. 2010. Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus. Plant Molecular Biology 73: 143-156.
Kramer MF. 2011. Stem-loop RT-qPCR for miRNAs. Current Protocols in Molecular Biology 95: 15.10.
Lal S, Pacis LB, Smith HM. 2011. Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 module by the homeodomain proteins PENNYWISE and POUND-FOOLISH in Arabidopsis. Molecular Plant 4: 1123-1132.
Lawrence EH, Leichty AR, Doody EE, Ma C, Strauss SH, Poethig RS. 2021. Vegetative phase change in Populus tremula × alba. New Phytologist 231: 351-364.
Leivar P, Quail PH. 2011. PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science 16: 19-28.
Li C, Lu S. 2014. Molecular characterization of the SPL gene family in Populus trichocarpa. BMC Plant Biology 14: 131.
Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H. 2007. Transposase-derived transcription in Arabidopsis. Science 318: 1302-1305.
Liu Y, Wu G, Zhao Y, Wang HH, Dai Z, Xue W, Yang J, Wei H, Shen R, Wang H. 2021. DWARF53 interacts with transcription factors UB2/UB3/TSH4 to regulate maize tillering and tassel branching. Plant Physiology 187: 947-962.
de Lucas M, Prat S. 2014. PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. New Phytologist 202: 1126-1141.
Maurya JP, Bhalerao RP. 2017. Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective. Annals of Botany 120: 351-360.
Maurya JP, Miskolczi PC, Mishra S, Singh RK, Bhalerao RP. 2020a. A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. Proceedings of the National Academy of Sciences, USA 117: 11523-11530.
Maurya JP, Singh RK, Miskolczi PC, Prasad AN, Jonsson K, Wu F, Bhalerao RP. 2020b. Branching regulator BRC1 mediates photoperiodic control of seasonal growth in hybrid aspen. Current Biology 30: 122-126.
Miskolczi P, Singh RK, Tylewicz S, Azeez A, Maurya JP, Tarkowská D, Novák O, Jonsson K, Bhalerao RP. 2019. Long-range mobile signals mediate seasonal control of shoot growth. Proceedings of the National Academy of Sciences, USA 166: 10852-10857.
Muhr M, Paulat M, Awwanah M, Brinkkötter M, Teichmann T. 2018. CRISPR/Cas9-mediated knockout of Populus BRANCHED1 and BRANCHED2 orthologs reveals a major function in bud outgrowth control. Tree Physiology 38: 1588-1597.
Muhr M, Prüfer N, Paulat M, Teichmann T. 2016. Knockdown of strigolactone biosynthesis genes in Populus affects BRANCHED1 expression and shoot architecture. New Phytologist 212: 613-626.
Ramos-Sánchez JM, Triozzi PM, Alique D, Geng F, Gao M, Jaeger KE, Wigge PA, Allona I, Perales M. 2019. LHY2 integrates night-length information to determine timing of poplar photoperiodic growth. Current Biology 29: 2402-2406.
Rohde A, Storme V, Jorge V, Gaudet M, Vitacolonna N, Fabbrini F, Ruttink T, Zaina G, Marron N, Dillen S et al. 2011. Bud set in poplar - genetic dissection of a complex trait in natural and hybrid populations. New Phytologist 189: 106-121.
Singh RK, Bhalerao RP, Eriksson ME. 2021. Growing in time: exploring the molecular mechanisms of tree growth. Tree Physiology 41: 657-678.
Singh RK, Maurya JP, Azeez A, Miskolczi P, Tylewicz S, Stojkovič K, Delhomme N, Busov V, Bhalerao RP. 2018. A genetic network mediating the control of bud break in hybrid aspen. Nature Communications 9: 4173.
Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A, Singh RK, Immanen J, Mähler N, Hvidsten TR, Eklund DM et al. 2018. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science 360: 212-215.
Tylewicz S, Tsuji H, Miskolczi P, Petterle A, Azeez A, Jonsson K, Shimamoto K, Bhalerao RP. 2015. Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways. Proceedings of the National Academy of Sciences, USA 112: 3140-3145.
Wang H, Wang H. 2015. The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Molecular Plant 8: 677-688.
Wang J, Yu H, Xiong G, Lu Z, Jiao Y, Meng X, Liu G, Chen X, Wang Y, Li J. 2017. Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN1 modulates IPA1 protein levels to regulate plant architecture in rice. Plant Cell 29: 697-707.
Wang JW, Czech B, Weigel D. 2009. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749.
Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS. 2011. MiRNA control of vegetative phase change in trees. PLoS Genetics 7: 21-25.
Wei H, Zhao Y, Xie Y, Wang H. 2018. Exploiting SPL genes to improve maize plant architecture tailored for high-density planting. Journal of Experimental Botany 69: 4675-4688.
Wu G, Poethig RS. 2006. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539-3547.
Xie Y, Liu Y, Ma M, Zhou Q, Zhao Y, Zhao B, Wang B, Wei H, Wang H. 2020a. Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching. Nature Communications 11: 1955.
Xie Y, Liu Y, Wang H, Ma X, Wang B, Wu G, Wang H. 2017. Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nature Communications 8: 348.
Xie Y, Zhou Q, Zhao Y, Li Q, Liu Y, Ma M, Wang B, Shen R, Zheng Z, Wang H. 2020b. FHY3 and FAR1 integrate light signals with the miR156-SPL module-mediated aging pathway to regulate Arabidopsis flowering. Molecular Plant 13: 483-498.
Xu M, Hu T, Poethig RS. 2021. Low light intensity delays vegetative phase change. Plant Physiology 187: 1177-1188.
Xu M, Hu T, Zhao J, Park MY, Earley KW, Wu G, Yang L, Poethig RS. 2016. Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in Arabidopsis thaliana. PLoS Genetics 12: e1006263.
Yang J, Wei H, Hou M, Chen L, Zou T, Ding H, Jing Y, Zhang X, Zhao Y, Liu Q et al. 2023. ZmSPL13 and ZmSPL29 act together to promote vegetative and reproductive transition in maize. New Phytologist 239: 1505-1520.