Regulation of storage organ formation by long-distance tuberigen signals in potato

Abstract

Potatoes are valued as reliable crops due to their high carbohydrate content and relatively low farming demands. Consequently, significant attention has been directed towards understanding and controlling the life cycle of potato tubers in recent years. Notably, recent studies have identified self-pruning 6A (StSP6A) as a key component of the tuberigen, the mobile signal for tuber formation, produced in leaves and then transported underground to induce tuber formation in potatoes. Recent progress in comprehending the signaling mechanisms that regulate StSP6A by photoperiod and ambient temperature components, its long-distance transport into underground tissue, and its involvement in regulating stolon tuberization has advanced significantly. Consequently, the modulation of StSP6A and other possible tuberigen signals, along with their regulatory pathways, significantly impacts potato domestication and crop yield. This progress highlights the differential regulation of tuberigen signals and their potential functions in promoting tuber formation.

Acknowledgements

The authors would like to thank Lijie Xuan, Meiqi Shi, Yupeng Jiang, Shiyu Jiang for their helpful discussions and comments on the manuscript. This work was supported by the Shanghai Collaborative Innovation Center of Agri-Seeds (ZXWH2150201/013), the National Natural Science Fund of China (32072119), Chinese Academy of Agricultural Sciences Innovation Project (CAAS-ASTIP-IVFCAAS).

Author contributions

L.L. and G.L. conceived and designed this review article. X.B. wrote the manuscript and designed and prepared the figs. Y.Z. provided comments and offered professional assistance. L.L. and G.L. made extensive revisions and generated the final version. All authors read and approved the final version of the manuscript.

Data availability

No application to this article as no datasets were generated or analyzed during the current study.

Conflict of interests

The authors declare no competing interests.

References

[1] Stokstad E. The new potato. Science. 2019; 363:574-7

[2] Abelenda JA, Navarro C, Prat S. From the model to the crop: genes controlling tuber formation in potato. Curr Opin Biotech-nol. 2011; 22:287-92

[3] Dolniˇcar P. Importance of potato as a crop and practical approaches to potato breeding. Methods Mol Biol. 2021; 2354:3-20

[4] Qu L, Huang X, Su X. et al. Potato: from functional genomics to genetic improvement. Mol Hortic. 2024; 4:34

[5] Gervais T, Creelman A, Li XQ. et al. Potato response to drought stress: physiological and growth basis. Front Plant Sci. 2021; 12:698060

[6] Liang S-M, Li Y-S, Rashid MAR. et al. Effects of planting pat-terns on rainwater use efficiency and potato tuber yield in seasonally arid areas of southwestern China. Soil Tillage Res. 2020; 197:104502

[7] Xu X, van Lammeren AA, Vermeer E. et al. The role of gib-berellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol. 1998; 117:575-84

[8] Xu X, Vreugdenhil D. van Lammeren AA. Cell division and cell enlargement during potato tuber formation. JExp Bot. 1998; 49: 573-82

[9] Reeve RM, Hautala E, Weaver ML. Anatomy and compositional variation within potatoes. Am Potato J. 1969; 46:361-73

[10] Zierer W, Ruscher D, Sonnewald U. et al. Tuber and tuberous root development. Annu Rev Plant Biol. 2021; 72:551-80

[11] Liu L, Xuan L, Jiang Y. et al. Regulation by FLOWERING LOCUS T and TERMINAL FLOWER 1 in flowering time and plant archi-tecture. Small Struct. 2021; 2:2000125

[12] Jin S, Nasim Z, Susila H. et al. Evolution and functional diver-sification of FLOWERING LOCUS T/TERMINAL FLOWER 1 family genes in plants. Semin Cell Dev Biol. 2021; 109:20-30

[13] Wickland DP, Hanzawa Y. The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant. 2015; 8:983-97

[14] Abelenda JA, Navarro C, Prat S. Flowering and tuberization: a tale of two nightshades. Trends Plant Sci. 2014; 19:115-22

[15] Gancarz M, Konstankiewicz K, Zgórska K. Cell orientation in potato tuber parenchyma tissue. Int Agrophys. 2014; 28:15-22

[16] Viola R, Roberts AG, Haupt S. et al. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell. 2001; 13:385-98

[17] Hancock RD, Roberts AG, Viola R. A role for symplastic gating in the control of the potato tuber life cycle. Plant Signal Behav. 2008; 3:27-9

[18] Zrenner R, Salanoubat M, Willmitzer L. et al. Evidence of the crucial role of sucrose synthase for sink strength using trans-genic potato plants (Solanum tuberosum L.). Plant J. 1995; 7:97-107

[19] Yang R, Sun Y, Zhu X. et al. The tuber-specific StbHLH93 gene regulates proplastid-to-amyloplast development during stolon swelling in potato. New Phytol. 2024; 241:1676-89

[20] Rodríguez-Falcón M, Bou J, Prat S. Seasonal control of tuber-ization in potato: conserved elements with the flowering response. Annu Rev Plant Biol. 2006; 57:151-80

[21] Jackson SD. Multiple signaling pathways control tuber induc-tion in potato. Plant Physiol. 1999; 119:1-8

[22] Ai Y, Jing S, Cheng Z. et al. DNA methylation affects photoperi-odic tuberization in potato (Solanum tuberosum L.) by mediating the expression of genes related to the photoperiod and GA pathways. Hortic Res. 2021; 8:181

[23] Zeevaart JAD. Physiology of flower formation. Annu Rev Plant Physiol. 1976; 27:321-48

[24] Navarro C, Abelenda JA, Cruz-Oro E. et al. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature. 2011; 478:119-22

[25] Lee R, Baldwin S, Kenel F. et al. FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat Commun. 2013; 4:2884

[26] Wang Y, Liu L, Song S. et al. DOFT and DOFTIP1 affect reproduc-tive development in the orchid Dendrobium chao Praya smile. JExp Bot. 2017; 68:5759-72

[27] Andres F, Coupland G. The genetic basis of flowering responses to seasonal cues. Nat Rev Genet. 2012; 13:627-39

[28] Bhogale S, Mahajan AS, Natarajan B. et al. MicroRNA156: a potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andi-gena. Plant Physiol. 2014; 164:1011-27

[29] Martin A, Adam H, Díaz-Mendoza M. et al. Graft-transmissible induction of potato tuberization by the microRNA miR172. Development. 2009; 136:2873-81

[30] Sharma P, Lin T, Hannapel DJ. Targets of the StBEL5 tran-scription factor include the FT ortholog StSP6A. Plant Physiol. 2016; 170:310-24

[31] Hannapel DJ, Sharma P, Lin T. et al. The multiple signals that control tuber formation. Plant Physiol. 2017; 174:845-56

[32] Abelenda JA, Cruz-Oro E, Franco-Zorrilla JM. et al. Potato StCONSTANS-like1 suppresses storage organ formation by directly activating the FT-like StSP5G repressor. Curr Biol. 2016; 26:872-81

[33] Zhou T, Song B, Liu T. et al. Phytochrome F plays critical roles in potato photoperiodic tuberization. Plant J. 2019; 98:42-54

[34] Kloosterman B, Abelenda JA, Gomez Mdel M. et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature. 2013; 495:246-50

[35] Hancock RD, Morris WL, Ducreux LJ. et al. Physiological, bio-chemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ. 2014; 37:439-50

[36] Morris WL, Ducreux LJM, Morris J. et al. Identification of TIMING OF CAB EXPRESSION 1 as a temperature-sensitive negative regulator of tuberization in potato. JExp Bot. 2019; 70:5703-14

[37] Lehretz GG, Sonnewald S, Hornyik C. et al. Post-transcriptional regulation of FLOWERING LOCUS T modulates heat-dependent source-sink development in potato. Curr Biol. 2019; 29:1614-1624 e3

[38] Martínez-García JF, Virgos-Soler A, Prat S. Control of photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time gene CONSTANS. Proc Natl Acad Sci USA. 2002; 99:15211-6

[39] González-Schain ND, Díaz-Mendoza M, Zurczak M. et al. Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J. 2012; 70:678-90

[40] Fornara F, Panigrahi KC, Gissot L. et al. Arabidopsis DOF tran-scription factors act redundantly to reduce CONSTANS expres-sion and are essential for a photoperiodic flowering response. Dev Cell. 2009; 17:75-86

[41] Imaizumi T, Schultz TF, Harmon FG. et al. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science. 2005; 309:293-7

[42] Sawa M, Nusinow DA, Kay SA. et al. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science. 2007; 318:261-5

[43] Gutaker RM, Weiss CL, Ellis D. et al. The origins and adaptation of European potatoes reconstructed from historical genomes. Nat Ecol Evol. 2019; 3:1093-101

[44] Jackson SD, Heyer A, Dietze J. et al. Phytochrome B mediates the photoperiodic control of tuber formation in potato. Plant J. 2002; 9:159-66

[45] Jing S, Jiang P, Sun X. et al. Long-distance control of potato storage organ formation by SELF PRUNING 3D and FLOWERING LOCUS T-like 1. Plant Commun. 2023; 4:100547

[46] Zhang S, Jiao Z, Liu L. et al. Enhancer-promoter interaction of SELF PRUNING 5G shapes photoperiod adaptation. Plant Physiol. 2018; 178:1631-42

[47] Soyk S, Muller NA, Park SJ. et al. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet. 2017; 49:162-8

[48] Yuan J, Ott T, Hiltbrunner A. Phytochromes and flowering: legumes do it another way. Trends Plant Sci. 2023; 28:379-81

[49] Chen H, Banerjee AK, Hannapel DJ. The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J. 2004; 38:276-84

[50] Kondhare KR, Vetal PV, Kalsi HS. et al. BEL1-like protein (StBEL5) regulates CYCLING DOF FACTOR1 (StCDF1)through tandem TGAC core motifs in potato. J Plant Physiol. 2019; 241: 153014

[51] Menzel CM. Tuberization in potato at high temperatures: responses to gibberellin and growth inhibitors. Ann Bot. 1980; 46:259-65

[52] Wolf S, Marani A, Rudich J. Effects of temperature and pho-toperiod on assimilate partitioning in potato plants. Ann Bot. 1990; 66:513-20

[53] Singh A, Siddappa S, Bhardwaj V. et al. Expression profiling of potato cultivars with contrasting tuberization at elevated temperature using microarray analysis. Plant Physiol Biochem. 2015; 97:108-16

[54] Park JS, Park SJ, Kwon SY. et al. Temporally distinct regulatory pathways coordinate thermo-responsive storage organ forma-tion in potato. Cell Rep. 2022; 38:110579

[55] Liu L, Zhang Y, Yu H. Florigen trafficking integrates photope-riod and temperature signals in Arabidopsis. J Integr Plant Biol. 2020; 62:1385-98

[56] Pose D, Verhage L, Ott F. et al. Temperature-dependent reg-ulation of flowering by antagonistic FLM variants. Nature. 2013; 503:414-7

[57] Lee JH, Ryu HS, Chung KS. et al. Regulation of temperature-responsive flowering by MADS-box transcription factor repres-sors. Science. 2013; 342:628-32

[58] Kumar SV, Lucyshyn D, Jaeger KE. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 2012; 484:242-5

[59] Blazquez MA, Ahn JH, Weigel D. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet. 2003; 33:168-71

[60] Hastilestari BR, Lorenz J, Reid S. et al. Deciphering source and sink responses of potato plants (Solanum tuberosum L.) to ele-vated temperatures. Plant Cell Environ. 2018; 41:2600-16

[61] Wu L, Liu D, Wu J. et al. Regulation of FLOWERING LOCUS T by a microRNA in Brachypodium distachyon. Plant Cell. 2013; 25: 4363-77

[62] Reynolds MP, Ewing EE. Effects of high air and soil temperature stress on growth and tuberization in Solanum tuberosum. Ann Bot. 1989; 64:241-7

[63] Stephen DJ, Pat J, Prat S. et al. Phytochrome B affects the levels of a graft-transmissible signal involved in tuberization. Plant Physiol. 1998; 117:29-32

[64] Tang D, Jia Y, Zhang J. et al. Genome evolution and diversity of wild and cultivated potatoes. Nature. 2022; 606:535-41

[65] Plantenga FDM, Bergonzi S, Abelenda JA. et al. The tuberization signal StSP6A represses flower bud development in potato. JExp Bot. 2019; 70:937-48

[66] Hay A, Tsiantis M. KNOX genes: versatile regulators of plant development and diversity. Development. 2010; 137:3153-65

[67] Banerjee AK, Chatterjee M, Yu Y. et al. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell. 2006; 18:3443-57

[68] Cho SK, Sharma P, Butler NM. et al. Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. JExp Bot. 2015; 66:6835-47

[69] Banerjee AK, Lin T, Hannapel DJ. Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol. 2009; 151:1831-43

[70] Chatterjee M, Banerjee AK, Hannapel DJ. A BELL1-like gene of potato is light activated and wound inducible. Plant Physiol. 2007; 145:1435-43

[71] Lin T, Sharma P, Gonzalez DH. et al. The impact of the long-distance transport of a BEL1-like messenger RNA on develop-ment. Plant Physiol. 2013; 161:760-72

[72] Wu G, Park MY, Conway SR. et al. The sequential action of miR156 and miR172 regulates developmental timing in Ara-bidopsis. Cell. 2009; 138:750-9

[73] Taoka K, Ohki I, Tsuji H. et al. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature. 2011; 476:332-5

[74] Abe M, Kobayashi Y, Yamamoto S. et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 2005; 309:1052-6

[75] Teo CJ, Takahashi K, Shimizu K. et al. Potato tuber induction is regulated by interactions between components of a tuberigen complex. Plant Cell Physiol. 2017; 58:365-74

[76] Jing S, Sun X, Yu L. et al. Transcription factor StABI5-like 1 binding to the FLOWERING LOCUS T homologs promotes early maturity in potato. Plant Physiol. 2022; 189:1677-93

[77] Sun X, Wang E, Yu L. et al. TCP transcription factor StAST1 represses potato tuberization by regulating tuberigen complex activity. Plant Physiol. 2024; 195:1347-64

[78] Eshed Y, Lippman ZB. Revolutions in agriculture chart a course for targeted breeding of old and new crops. Science. 2019; 366: eaax0025

[79] Prusinkiewicz P, Erasmus Y, Lane B. et al. Evolution and development of inflorescence architectures. Science. 2007; 316: 1452-6

[80] Teo ZW, Song S, Wang YQ. et al. New insights into the regu-lation of inflorescence architecture. Trends Plant Sci. 2014; 19: 158-65

[81] Zhu Y, Klasfeld S, Jeong CW. et al. TERMINAL FLOWER 1-FD complex target genes and competition with FLOWERING LOCUS T. Nat Commun. 2020; 11:5118

[82] Zhang X, Campbell R, Ducreux LJM. et al. TERMINAL FLOWER-1/CENTRORADIALIS inhibits tuberisation via protein interac-tion with the tuberigen activation complex. Plant J. 2020; 103: 2263-78

[83] Corbesier L, Vincent C, Jang S. et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science. 2007; 316:1030-3

[84] Jaeger KE, Wigge PA. FT protein acts as a long-range signal in Arabidopsis. Curr Biol. 2007; 17:1050-4

[85] Mathieu J, Warthmann N, Kuttner F. et al. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol. 2007; 17:1055-60

[86] Notaguchi M, Abe M, Kimura T. et al. Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T pro-tein to promote flowering. Plant Cell Physiol. 2008; 49:1645-58

[87] Wang E, Zhou T, Jing S. et al. Leaves and stolons transcrip-tomic analysis provide insight into the role of phytochrome F in potato flowering and tuberization. Plant J. 2023; 113: 402-15

[88] Liu L, Liu C, Hou X. et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 2012; 10:e1001313

[89] Kloosterman B, Navarro C, Bijsterbosch G. et al. StGA2ox1 is induced prior to stolon swelling and controls GA levels during potato tuber development. Plant J. 2007; 52:362-73

[90] Kloosterman B, Vorst O, Hall RD. et al. Tuber on a chip: differ-ential gene expression during potato tuber development. Plant Biotechnol J. 2005; 3:505-19

[91] Hartmann A, Senning M, Hedden P. et al. Reactivation of meris-tem activity and sprout growth in potato tubers require both cytokinin and gibberellin. Plant Physiol. 2011; 155:776-96

[92] Lehretz GG, Sonnewald S, Sonnewald U. Assimilate highway to sink organs - physiological consequences of SP6A overexpres-sion in transgenic potato (Solanum tuberosum L.). J Plant Physiol. 2021; 266:153530

[93] Abelenda JA, Bergonzi S, Oortwijn M. et al. Source-sink regula-tion is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr Biol. 2019; 29:1178-1186 e6

[94] Nicolas M, Torres-Perez R, Wahl V. et al. Spatial control of potato tuberization by the TCP transcription factor BRANCHED1b. Nat Plants. 2022; 8:281-94

[95] Roumeliotis E, Kloosterman B, Oortwijn M. et al. Down regula-tion of StGA3ox genes in potato results in altered GA content and affect plant and tuber growth characteristics. J Plant Physiol. 2013; 170:1228-34

[96] Carrera E, Bou J, Garcia-Martinez JL. et al. Changes in GA 20-oxidase gene expression strongly affect stem length, tuber induction and tuber yield of potato plants. Plant J. 2000; 22: 247-56

[97] Roumeliotis E, Visser RG, Bachem CW. A crosstalk of auxin and GA during tuber development. Plant Signal Behav. 2012; 7:1360-3

[98] Kondhare KR, Patil AB, Giri AP. Auxin: an emerging regulator of tuber and storage root development. Plant Sci. 2021; 306: 110854

[99] Roumeliotis E, Kloosterman B, Oortwijn M. et al. The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. JExp Bot. 2012; 63:4539-47

[100] Guivarc’h A, Rembur J, Goetz M. et al. Local expression of the ipt gene in transgenic tobacco (Nicotiana tabacum L. cv. SR1) axillary buds establishes a role for cytokinins in tuberization and sink formation. JExp Bot. 2002; 53:621-9

[101] Eviatar-Ribak T, Shalit-Kaneh A, Chappell-Maor L. et al. A cytokinin-activating enzyme promotes tuber formation in tomato. Curr Biol. 2013; 23:1057-64

[102] Deng R, Huang S, Du J. et al. The brassinosteroid receptor StBRI1 promotes tuber development by enhancing plasma membrane H+-ATPase activity in potato. Plant Cell. 2024; 36: 3498-520

[103] Kuhn C, Grof CP. Sucrose transporters of higher plants. Curr Opin Plant Biol. 2010; 13:288-98

[104] Chen LQ, Qu XQ, Hou BH. et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012; 335:207-11

[105] Chincinska IA, Liesche J, Krugel U. et al. Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol. 2008; 146:515-28

[106] Huang X, Zhao P, Peng X. et al. Seed development in Ara-bidopsis: what we have learnt in the past 30 years. Seed Biol. 2023; 2:6

[107] Xu G, Zhang X. Mechanisms controlling seed size by early endosperm development. Seed Biol. 2023; 2:1-11

[108] Zhou YF, Qing T, Shu XL. et al. Unfolded protein response and storage product accumulation in rice grains. Seed Biol. 2022; 1:1-5

[109] Zhang L, Zhang F, Zhou X. et al. The tetratricopeptide repeat protein OsTPR075 promotes heading by regulating florigen transport in rice. Plant Cell. 2022; 34:3632-46

[110] Song S, Chen Y, Liu L. et al. OsFTIP1-mediated regula-tion of florigen transport in rice is negatively regulated by the ubiquitin-like domain kinase OsUbDKgamma4. Plant Cell. 2017; 29:491-507

[111] Susila H, Juric S, Liu L. et al. Florigen sequestration in cellular membranes modulates temperature-responsive flowering. Sci-ence. 2021; 373:1137-42

[112] Liu L, Li C, Teo ZWN. et al. The MCTP-SNARE complex regulates florigen transport in Arabidopsis. Plant Cell. 2019; 31:2475-90

[113] Mathura SR, Sutton F, Rouse-Miller J. et al. The molecular coor-dination of tuberization: current status and future directions. Curr Opin Plant Biol. 2024; 82:102655

[114] Hardigan MA, Laimbeer FPE, Newton L. et al. Genome diversity of tuber-bearing solanum uncovers complex evolutionary his-tory and targets of domestication in the cultivated potato. Proc Natl Acad Sci USA. 2017; 114:E9999-10008

[115] Zhang F, Qu L, Gu Y. et al. Resequencing and genome-wide association studies of autotetraploid potato. Mol Hortic. 2022; 2:6

[116] Wu Y, Li D, Hu Y. et al. Phylogenomic discovery of dele-terious mutations facilitates hybrid potato breeding. Cell. 2023; 186:2313-2328 e15

[117] Zhang C, Wang P, Tang D. et al. The genetic basis of inbreeding depression in potato. Nat Genet. 2019; 51:374-8