Spatiotemporal miRNA and transcriptomic network dynamically regulate the developmental and senescence processes of poplar leaves

Kang Du , Shenxiu Jiang , Hao Chen , Yufei Xia , Ruihua Guo , Aoyu Ling , Ting Liao , Wenqi Wu , Xiangyang Kang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (10) : 186

PDF (2464KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (10) :186 DOI: 10.1093/hr/uhad186
Article
research-article
Spatiotemporal miRNA and transcriptomic network dynamically regulate the developmental and senescence processes of poplar leaves
Author information +
History +
PDF (2464KB)

Abstract

Poplar is an important afforestation and urban greening species. Poplar leaf development occurs in stages, from young to mature and then from mature to senescent; these are accompanied by various phenotypic and physiological changes. However, the associated transcriptional regulatory network is relatively unexplored. We first used principal component analysis to classify poplar leaves at different leaf positions into two stages: developmental maturity (the stage of maximum photosynthetic capacity); and the stage when photosynthetic capacity started to decline and gradually changed to senescence. The two stages were then further subdivided into five intervals by gene expression clustering analysis: young leaves, the period of cell genesis and functional differentiation (L1); young leaves, the period of development and initial formation of photosynthetic capacity (L3–L7); the period of maximum photosynthetic capacity of functional leaves (L9–L13); the period of decreasing photosynthetic capacity of functional leaves (L15–L27); and the period of senescent leaves (L29). Using a weighted co-expression gene network analysis of regulatory genes, high-resolution spatiotemporal transcriptional regulatory networks were constructed to reveal the core regulators that regulate leaf development. Spatiotemporal transcriptome data of poplar leaves revealed dynamic changes in genes and miRNAs during leaf development and identified several core regulators of leaf development, such as GRF5 and MYB5. This in-depth analysis of transcriptional regulation during leaf development provides a theoretical basis for exploring the biological basis of the transcriptional regulation of leaf development and the molecular design of breeding for delaying leaf senescence.

Cite this article

Download citation ▾
Kang Du, Shenxiu Jiang, Hao Chen, Yufei Xia, Ruihua Guo, Aoyu Ling, Ting Liao, Wenqi Wu, Xiangyang Kang. Spatiotemporal miRNA and transcriptomic network dynamically regulate the developmental and senescence processes of poplar leaves. Horticulture Research, 2023, 10 (10) : 186 DOI:10.1093/hr/uhad186

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This research was supported by the National Key R&D Program of China during the 14th Five-year Plan Period (2021YFD2200105).

Author contributions

X.Y.K., T.L., and K.D. conceived and designed the experiments. K.D., S.X.J., R.H.G., A.Y.L., Y.F.X., and H.C. performed the experiments. K.D. wrote the paper. W.Q.W., K.D., and X.Y.K. revised the manuscript. All authors read and approved the final version of the paper.

Data availability

The supplementary information that accompanies this article can be found on the Horticulture Research website. RNA-sequencing data in this study have been deposited in the CNCB Bioproject database under accession number CRA011796.

Conflict of interest

The authors declare no competing financial interests.

References

[1]

Myneni RB, Dong J, Tucker CJ et al. A large carbon sink in the woody biomass of northern forests. Proc Natl Acad Sci USA. 2001; 98: 14784-9

[2]

Wu Y, Cai Y, Yang F et al. Chemical modification of poplar wood featuring compressible rebound 3D structure as water treatment absorbents. J Clean Prod. 2022; 331: 129952

[3]

Wang W, Chen K, Chen N et al. Chromatin accessibility dynamics insight into crosstalk between regulatory landscapes in poplar responses to multiple treatments. Tree Physiol. 2023; 43: 1023-41

[4]

Vialet-Chabrand S, Matthews JSA, Simkin AJ et al. Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol. 2017; 173: 2163-79

[5]

Gary J, Proebsting E . The multiple landscapes of Thomas Jefferson’s poplar forest. Hist Archaeol. 2016; 50: 61-79

[6]

Woo HR, Koo HJ, Kim J et al. Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiol. 2016; 171: 452-67

[7]

Fleming AJ . The control of leaf development. New Phytol. 2005; 166: 9-20

[8]

Breeze E, Harrison E, McHattie S et al. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell. 2011; 23: 873-94

[9]

Meng X, Zhang P, Chen Q et al. Identification and characterization of ncRNA-associated ceRNA networks in Arabidopsis leaf development. BMC Genomics. 2018; 19: 607-10

[10]

Kim J, Kim JH, Lyu JI et al. New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot. 2018; 69: 787-99

[11]

Huang J, Li Z, Zhao D . Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Sci Rep. 2016; 6: 1-14

[12]

Omidbakhshfard MA, Proost S, Fujikura U et al. Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant. 2015; 8: 998-1010

[13]

Robert-Seilaniantz A, MacLean D, Jikumaru Y et al. The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J. 2011; 67: 218-31

[14]

Wu W, Li J, Wang Q et al. Growth-regulating factor 5 (GRF5)-mediated gene regulatory network promotes leaf growth and expansion in poplar. New Phytol. 2021; 230: 612-28

[15]

Zhao Y, Zhang Y, Zhang W et al. The PagKNAT2/6b-PagBOP1/2a regulatory module controls leaf morphogenesis in Populus. Int J Mol Sci. 2022; 23: 1-15

[16]

Samad AFA, Sajad M, Nazaruddin N et al. MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci. 2017; 8: 1-18

[17]

Wu W, Du K, Kang X et al. The diverse roles of cytokinins in regulating leaf development. Hortic Res. 2021; 8: 118

[18]

Garcês HMP, Champagne CEM, Townsley BT et al. Evolution of asexual reproduction in leaves of the genus Kalanchoë. Proc Natl Acad Sci USA. 2007; 104: 15578-83

[19]

Wang HL, Zhang Y, Wang T et al. An alternative splicing variant of PtRD26 delays leaf senescence by regulating multiple NAC transcription factors in Populus. Plant Cell. 2021; 33: 1594-614

[20]

Xu Y, Jin W, Li N et al. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis. Plant Cell. 2016; 28: 1200-14

[21]

Schommer C, Debernardi JM, Bresso EG et al. Repression of cell proliferation by miR319-regulated TCP4. Mol Plant. 2014; 7: 1533-44

[22]

Wang Y, Liu W, Wang X et al. MiR156 regulates anthocyanin biosynthesis through SPL targets and other microRNAs in poplar. Hortic Res. 2020; 7: 118

[23]

Vercruysse J, Baekelandt A, Gonzalez N et al. Molecular networks regulating the cell division during leaf growth in Arabidopsis. J Exp Bot. 2019; 71: 2365-78

[24]

Futschik ME . Introduction to Mfuzz package and its graphical user interface. Analysis. 2009; 2: 5-7

[25]

Ren M, Zhang Y, Liu C et al. Characterization of a high hierarchical regulator, PtrGATA12, functioning in differentially regulating secondary wall component biosynthesis in Populus trichocarpa. Front Plant Sci. 2021; 12: 657787

[26]

Yolcu S, Li X, Li S et al. Beyond the genetic code in leaf senescence. J Exp Bot. 2018; 69: 801-10

[27]

Yoshida K, Ma D, Constabel CP . The MYB182 protein downregulates proanthocyanidin and anthocyanin biosynthesis in poplar by repressing both structural and regulatory flavonoid genes. Plant Physiol. 2015; 167: 693-710

[28]

Seki K, Komatsu K, Tanaka K et al. A CIN-like TCP transcription factor (LsTCP4) having retrotransposon insertion associates with a shift from Salinas type to Empire type in crisphead lettuce (Lactuca sativa L.). Hortic Res. 2020; 7: 15

[29]

Ma D, Reichelt M, Yoshida K et al. Two R2R3-MYB proteins are broad repressors of flavonoid and phenylpropanoid metabolism in poplar. Plant J. 2018; 96: 949-65

[30]

Kieffer M, Master V, Waites R et al. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis. Plant J. 2011; 68: 147-58

[31]

Zhao Y, Song X, Zhou H et al. KNAT2/6b, a class I KNOX gene, impedes xylem differentiation by regulating NAC domain transcription factors in poplar. New Phytol. 2020; 225: 1531-44

[32]

Kierzkowski D, Runions A, Vuolo F et al. A growth-based framework for leaf shape development and diversity. Cell. 2019; 177: 1405-1418.e17

[33]

Wai CM, VanBuren R, Zhang J et al. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. Plant J. 2017; 92: 19-30

[34]

Lu Y, Feng Z, Meng Y et al. SLENDER RICE1 and Oryza sativa INDETERMINATE DOMAIN2 regulating OsmiR396 are involved in stem elongation. Plant Physiol. 2020; 182: 2213-27

[35]

Ostrowska-Mazurek A, Kasprzak P, Kubala S et al. Epigenetic landmarks of leaf senescence and crop improvement. Int J Mol Sci. 2020; 21: 1-17

[36]

Wang J, Zhou H, Zhao Y et al. PagGRF12a interacts with PagGIF1b to regulate secondary xylem development through modulating PagXND1a expression in Populus alba × P. glandulosa. J Integr Plant Biol. 2021; 63: 1683-94

[37]

Vadde BVL, Challa KR, Nath U . The TCP4 transcription factor regulates trichome cell differentiation by directly activating GLABROUS INFLORESCENCE STEMS in Arabidopsis thaliana. Plant J. 2018; 93: 259-69

[38]

Zheng X, Lan J, Yu H et al. Arabidopsis transcription factor TCP4 represses chlorophyll biosynthesis to prevent petal greening. Plant Commun. 2022; 3: 100309

[39]

Omidbakhshfard MA, Fujikura U, Olas JJ et al. GROWTH-REGULATING FACTOR 9 negatively regulates Arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia. 2018; 14: e1007484

[40]

Cheng S, Yang J, Liao T et al. Transcriptomic changes following synthesis of a Populus full-sib diploid and allotriploid population with different heterozygosities driven by three types of 2n female gamete. Plant Mol Biol. 2015; 89: 493-510

[41]

Wang S, Yang H, Mei J et al. Rice homeobox protein KNAT7 integrates the pathways regulating cell expansion and wall stiffness. Plant Physiol. 2019; 181: 669-82

[42]

Guo J, Bai X, Dai K et al. Identification of GATA transcription factors in Brachypodium distachyon and functional characterization of BdGATA13 in drought tolerance and response to gibberellins. Front Plant Sci. 2021; 12: 1-13

[43]

An Y, Zhou Y, Han X et al. A GATA transcription factor PdGNC plays an important role in photosynthesis and growth in polar. J Exp Bot. 2019; 71: 1969-84

[44]

Livak KJ, Schmittgen TD . Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25: 402-8

[45]

Li C, Pei J, Yan X et al. A poplar B-box protein PtrBBX23 modulates the accumulation of anthocyanins and proanthocyanidins in response to high light. Plant Cell Environ. 2021; 44: 3015-33

PDF (2464KB)

42

Accesses

0

Citation

Detail

Sections
Recommended

/