Abstract
Main conclusion
PdeHCA2 regulates the transition from primary to secondary growth, plant architecture, and affects photosynthesis by targeting PdeBRC1 and controlling the anatomy of the mesophyll, and intercellular space, respectively.
Abstract
Branching, secondary growth, and photosynthesis are vital developmental processes of woody plants that determine plant architecture and timber yield. However, the mechanisms underlying these processes are unknown. Here, we report that the Populus transcription factor High Cambium Activity 2 (PdeHCA2) plays a role in the transition from primary to secondary growth, vascular development, and branching. In Populus, PdeHCA2 is expressed in undifferentiated provascular cells during primary growth, in phloem cells during secondary growth, and in leaf veins, which is different from the expression pattern of its homolog in Arabidopsis. Overexpression of PdeHCA2 has pleiotropic effects on shoot and leaf development; overexpression lines showed delayed growth of shoots and leaves, reduced photosynthesis, and abnormal shoot branching. In addition, auxin-, cytokinin-, and photosynthesis-related genes were differentially regulated in these lines. Electrophoretic mobility shift assays and transcriptome analysis indicated that PdeHCA2 directly up-regulates the expression of BRANCHED1 and the MADS-box gene PdeAGL9, which regulate plant architecture, by binding to cis-elements in the promoters of these genes. Taken together, our findings suggest that HCA2 regulates several processes in woody plants including vascular development, photosynthesis, and branching by affecting the proliferation and differentiation of parenchyma cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data related to this manuscript can be found within this paper and its Supplementary data.
Abbreviations
- Ci:
-
Intracellular carbon dioxide concentration
- CK:
-
Cytokinin
- DEG:
-
Differentially expressed gene
- GO:
-
Gene ontology
- HCA :
-
High cambial activity
- IN:
-
Internode
- LPI:
-
Leaf plastochron index
- Pn:
-
Net photosynthesis rate
- SAM:
-
Shoot apical meristem
- TF:
-
Transcription factor
References
Abel S, Theologis A (1994) Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J 5(3):421–427. https://doi.org/10.1111/j.1365-313x.1994.00421.x
Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19(2):458–472. https://doi.org/10.1105/tpc.106.048934
Alexa A, Rahnenführer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22(13):1600–1607. https://doi.org/10.1093/bioinformatics/btl140
Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, Morelli G (2001) Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol 151(2):381–389. https://doi.org/10.1046/j.0028-646x.2001.00188.x
Alvarez JP, Furumizu C, Efroni I, Eshed Y, Bowman JL (2016) Active suppression of a leaf meristem orchestrates determinate leaf growth. Elife 5:e15023. https://doi.org/10.7554/eLife.15023
Anthony Little CH, MacDonald JE, Olsson O (2002) Involvement of indole-3-acetic acid in fascicular and interfascicular cambial growth and interfascicular extraxylary fiber differentiation in Arabidopsis thaliana inflorescence stems. Int J Plant Sci 163(4):519–529. https://doi.org/10.1086/339642
Baba K, Karlberg A, Schmidt J, Schrader J, Hvidsten TR, Bako L, Bhalerao RP (2011) Activity–dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Proc Natl Acad Sci USA 108(8):3418–3423. https://doi.org/10.1073/pnas.1011506108
Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA (2019) An update on the signals controlling shoot branching. Trends Plant Sci 24(3):220–236. https://doi.org/10.1016/j.tplants.2018.12.001
Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341(1):95–113. https://doi.org/10.1016/j.ydbio.2009.11.029
Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen Ari P, Helariutta Y (2011) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21(11):917–926. https://doi.org/10.1016/j.cub.2011.04.017
Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I (2008) A novel regulatory circuit underlying plant response to canopy shade. Plant Signal Behav 3(2):137–139
Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114(4):594–600. https://doi.org/10.1034/j.1399-3054.2002.1140413.x
Chao Q, Gao ZF, Zhang D, Zhao BG, Dong FQ, Fu CX, Liu LJ, Wang BC (2019) The developmental dynamics of the Populus stem transcriptome. Plant Biotech J 17(1):206–219. https://doi.org/10.1111/pbi.12958
Chaudhury AM, Letham S, Craig S, Dennis ES (1993) amp1 - a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4(6):907–916. https://doi.org/10.1046/j.1365-313X.1993.04060907.x
Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genom 11(1):150. https://doi.org/10.1186/1471-2164-11-150
Dixon LE, Greenwood JR, Bencivenga S, Zhang P, Cockram J, Mellers G, Ramm K, Cavanagh C, Swain SM, Boden SA (2018) TEOSINTE BRANCHED1 regulates inflorescence architecture and development in bread wheat Triticum aestivum. Plant Cell 30(3):563–581. https://doi.org/10.1105/tpc.17.00961
Dixon LE, Pasquariello M, Boden SA (2020) TEOSINTE BRANCHED1 regulates height and stem internode length in bread wheat. J Exp Bot 71(16):4742–4750. https://doi.org/10.1093/jxb/eraa252
Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386(6624):485–488. https://doi.org/10.1038/386485a0
Du J, Groover A (2010) Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52(1):17–27. https://doi.org/10.1111/j.1744-7909.2010.00901.x
Du J, Miura E, Robischon M, Martinez C, Groover A (2011) The Populus class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLoS One 6(2):e17458–e17458. https://doi.org/10.1371/journal.pone.0017458
Du F, Guan C, Jiao Y (2018) Molecular mechanisms of leaf morphogenesis. Mol Plant 11(9):1117–1134. https://doi.org/10.1016/j.molp.2018.06.006
Elo A, Immanen J, Nieminen K, Helariutta Y (2009) Stem cell function during plant vascular development. Semin Cell Dev Biol 20(9):1097–1106. https://doi.org/10.1016/j.semcdb.2009.09.009
Esau K (1954) Primary vascular differentiation in plants. Biol Rev 29(1):46–86. https://doi.org/10.1111/j.1469-185X.1954.tb01397.x
Fischer U, Kucukoglu M, Helariutta Y, Bhalerao RP (2019) The dynamics of cambial stem cell activity. Annu Rev Plant Biol 70(1):293–319. https://doi.org/10.1146/annurev-arplant-050718-100402
Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10(5):210–214. https://doi.org/10.1016/j.tplants.2005.03.001
Guo Y, Qin G, Gu H, Qu L-J (2009) Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21(11):3518–3534. https://doi.org/10.1105/tpc.108.064139
Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17(5):1405–1411. https://doi.org/10.1093/emboj/17.5.1405
Heintzen C, Fischer R, Melzer S, Kappeler S, Apel K, Staiger D (1994) Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol 106(3):905–915. https://doi.org/10.1104/pp.106.3.905
Hollender CA, Dardick C (2015) Molecular basis of angiosperm tree architecture. New Phytol 206(2):541. https://doi.org/10.1111/nph.13204
Horiguchi G, Kim G-T, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43(1):68–78. https://doi.org/10.1111/j.1365-313X.2005.02429.x
Hou J, Xu H, Fan D, Ran L, Li J, Wu S, Luo K, He XQ (2020) MiR319a-targeted PtoTCP20 regulates secondary growth via interactions with PtoWOX4 and PtoWND6 in Populus tomentosa. New Phytol 228(4):1354–1368. https://doi.org/10.1111/nph.16782
Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol 157(3):1151–1162. https://doi.org/10.1104/pp.111.185066
Immanen J, Nieminen K, Smolander OP, Kojima M, Serra JA, Koskinen P, Zhang J, Elo A, Mähönen AP, Street N, Bhalerao RP (2016) Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr Biol 26(15):1990–1997. https://doi.org/10.1016/j.cub.2016.05.053
Isebrands JG, Larson PR (1973) Anatomical changes during leaf ontogeny in Populus deltoides. Am J Bot 60(3):199–208. https://doi.org/10.1002/j.1537-2197.1973.tb10217.x
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58(1):435–458. https://doi.org/10.1146/annurev.arplant.58.032806.103956
Jiang L, Chen Y-B, Zheng J, Chen Z, Liu Y, Tao Y, Wu W, Chen Z, Wang B-C (2016) Structural basis of reversible phosphorylation by maize pyruvate orthophosphate dikinase regulatory protein. Plant Physiol 170(2):732–741. https://doi.org/10.1104/pp.15.01709
Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw982
Kishi-Kaboshi M, Muto H, Takeda A, Murata T, Hasebe M, Watanabe Y (2014) Localization of tobacco germin-like protein 1 in leaf intercellular space. Plant Physiol Biochem 85:1–8. https://doi.org/10.1016/j.plaphy.2014.10.005
Krebs J, Mueller-Roeber B, Ruzicic S (2010) A novel bipartite nuclear localization signal with an atypically long linker in DOF transcription factors. J Plant Physiol 167(7):583–586. https://doi.org/10.1016/j.jplph.2009.11.016
Lang GA (1987) Dormancy: a new universal terminology. HortScience 25:817–820
Larson PR (1975) Development and organization of the primary vascular system in Populus deltoides according to phyllotaxy. Am J Bot 62(10):1084–1099. https://doi.org/10.1002/j.1537-2197.1975.tb11774.x
Larson PR (1976) Procambium vs. cambium and protoxylem vs. metaxylem in Populus deltoides seedlings. Am J Bot 63(10):1332–1348. https://doi.org/10.2307/2441842
Larson PR (1994) The vascular cambium: development and structure. Springer Science and Business Media
Le Hir R, Bellini C (2013) The plant-specific Dof transcription factors family: new players involved in vascular system development and functioning in Arabidopsis. Front Plant Sci 4:164. https://doi.org/10.3389/fpls.2013.00164
Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100(8):4939–4944. https://doi.org/10.1073/pnas.0831166100
Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6(12):1859–1876. https://doi.org/10.1105/tpc.6.12.1859
Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JH (2014) Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat Commun 5:3767. https://doi.org/10.1038/ncomms4767
Lucas WJ, Groover A, Lichtenberger R et al (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55(4):294–388. https://doi.org/10.1111/jipb.12041
Ma X, Zhang Q, Zhu Q et al (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8(8):1274–1284. https://doi.org/10.1016/j.molp.2015.04.007
Ma D, Xu Y, Zhang Z, Li B, Chen T, Tian S (2018) Efficacy of ABA-mimicking ligands in controlling water loss and maintaining antioxidative capacity of Spinacia oleracea. J Agric Food Chem 66(51):13397–13404. https://doi.org/10.1021/acs.jafc.8b05859
Mandel MA, Yanofsky MF (1998) The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex Plant Reprod 11(1):22–28. https://doi.org/10.1007/s004970050116
Maurya JP, Miskolczi PC, Mishra S, Singh RK, Bhalerao RP (2020) A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. Proc Natl Acad Sci USA 117(21):11523–11530. https://doi.org/10.1073/pnas.2004705117
McAdam SAM, Eléouët MP, Best M et al (2017) Linking auxin with photosynthetic rate via leaf venation. Plant Physiol 175(1):351–360. https://doi.org/10.1104/pp.17.00535
Miyashima S, Roszak P, Sevilem I et al (2019) Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature 565(7740):490–494. https://doi.org/10.1038/s41586-018-0839-y
Nieminen K, Immanen J, Laxell M et al (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105(50):20032–20037. https://doi.org/10.1073/pnas.0805617106
Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding one zinc finger (DOF) transcription factor family in plants. Plant Sci 209:32–45. https://doi.org/10.1016/j.plantsci.2013.03.016
Ochando I, Jover-Gil S, Ripoll JJ, Candela H, Vera A, Ponce MR, Martinez-Laborda A, Micol JL (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in Arabidopsis. Plant Physiol 141(2):607–619. https://doi.org/10.1104/pp.106.077149
Ohashi-Ito K, Fukuda H (2014) Initiation of vascular development. Physiol Plant 151(2):142–146. https://doi.org/10.1111/ppl.12111
Parker G, Schofield R, Sundberg B, Turner S (2003) Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development 130(10):2139–2148. https://doi.org/10.1242/dev.00441
Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405(6783):200–203. https://doi.org/10.1038/35012103
Pineau C, Freydier A, Ranocha P et al (2005) hca: an Arabidopsis mutant exhibiting unusual cambial activity and altered vascular patterning. Plant J 44(2):271–289. https://doi.org/10.1111/j.1365-313X.2005.02526.x
Prassinos C, Ko J-H, Yang J, Han K-H (2005) Transcriptome profiling of vertical stem segments provides insights into the genetic regulation of secondary growth in hybrid aspen trees. Plant Cell Physiol 46(8):1213–1225. https://doi.org/10.1093/pcp/pci130
Richards E, Reichardt M, Rogers S (1994) Preparation of genomic DNA from plant tissue. Curr Protoc Mol Biol 27(1):231–237. https://doi.org/10.1002/0471142727.mb0203s27
Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110. https://doi.org/10.1126/science.290.5499.2105
Robischon M, Du J, Miura E, Groover A (2011) The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155(3):1214–1225. https://doi.org/10.1104/pp.110.167007
Ros Barceló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207(2):207–216. https://doi.org/10.1007/s004250050474
Sachs T, Thimann KV (1967) The role of auxins and cytokinins in the release of buds from dormancy. Am J Bot 54(1):136–144. https://doi.org/10.1002/j.1537-2197.1967.tb06901.x
Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131(14):3445–3455. https://doi.org/10.1242/dev.01182
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. Nat Commun 9(1):4173. https://doi.org/10.1038/s41467-018-06696-y
Smetana O, Makila R, Lyu M et al (2019) High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565(7740):485–489. https://doi.org/10.1038/s41586-018-0837-0
Smith LG, Greene B, Veit B, Hake S (1992) A dominant mutation in the maize homeobox gene, knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116(1):21–30
Sundell D, Street NR, Kumar M et al (2017) AspWood: high-spatial-resolution transcriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29(7):1585–1604. https://doi.org/10.1105/tpc.17.00153
Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2005) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57(2):343–354. https://doi.org/10.1093/jxb/erj014
Terashima I, Hanba YT, Tholen D, Niinemets Ü (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155(1):108–116. https://doi.org/10.1104/pp.110.165472
Tognetti VB, Bielach A, Hrtyan M (2017) Redox regulation at the site of primary growth: auxin, cytokinin and ROS crosstalk. Plant Cell Environ 40(11):2586–2605. https://doi.org/10.1111/pce.13021
Tsukaya H (2018) Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation. Semin Cell Dev Biol 79:48–57. https://doi.org/10.1016/j.semcdb.2017.11.035
Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604. https://doi.org/10.1126/science.1128691
Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20(3):648–657. https://doi.org/10.1105/tpc.107.054023
Vidaurre DP, Ploense S, Krogan NT, Berleth T (2007) AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134(14):2561–2567. https://doi.org/10.1242/dev.006759
Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12(5):527–538. https://doi.org/10.1016/j.pbi.2009.07.002
Wilson JW (1978) The position of regenerating cambia: auxin/sucrose ratio and the gradient induction hypothesis. Proc R Soc Lond Ser B, Biol Sci 203(1151):153–170. https://doi.org/10.1098/rspb.1978.0098
Xu C, Shen Y, He F et al (2019) Auxin-mediated Aux/IAA-ARF-HB signaling cascade regulates secondary xylem development in Populus. New Phytol 222(2):752–767. https://doi.org/10.1111/nph.15658
Zeng J, Dong Z, Wu H, Tian Z, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36(19):2844–2855. https://doi.org/10.15252/embj.201695955
Zhang X, Chen Y, Wang ZY, Chen Z, Gu H, Qu LJ (2007) Constitutive expression of CIR1 (RVE2) affects several circadian-regulated processes and seed germination in Arabidopsis. Plant J 51(3):512–525. https://doi.org/10.1111/j.1365-313X.2007.03156.x
Zhang X, Huai J, Shang F, Xu G, Tang W, Jing Y, Lin R (2017) A PIF1/PIF3-HY5-BBX23 transcription factor cascade affects photomorphogenesis. Plant Physiol 174(4):2487–2500. https://doi.org/10.1104/pp.17.00418
Zhong R, Ye Z-H (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11(11):2139–2152. https://doi.org/10.1105/tpc.11.11.2139
Zhu Y, Song D, Xu P, Sun J, Li L (2018) A HD-ZIP III gene, PtrHB4, is required for interfascicular cambium development in Populus. Plant Biotech J 16(3):808–817. https://doi.org/10.1111/pbi.12830
Acknowledgements
This work is supported by “The State Key Laboratory of Subtropical Silviculture” (Grant No. KF201903). We thank Dr. Melissa Lehti-Shiu (Lehti Life Science Editing) for proofreading the manuscript. This research was supported by the excellent platform of the Institute of Botany, The Chinese Academy of Sciences.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
425_2022_3883_MOESM2_ESM.xls
Supplementary file2 Annotation of differentially expressed genes from the shoot apex—IN3 stem RNA-sequencing data (XLS 497 KB)
425_2022_3883_MOESM4_ESM.xlsx
Supplementary file4 GO classification of the differentially expressed genes from the leaf and shoot apex—IN3 RNA-sequencing data (XLSX 51 KB)
Rights and permissions
About this article
Cite this article
Zhao, BG., Li, G., Wang, YF. et al. PdeHCA2 affects biomass in Populus by regulating plant architecture, the transition from primary to secondary growth, and photosynthesis. Planta 255, 101 (2022). https://doi.org/10.1007/s00425-022-03883-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-022-03883-6