Phloem development.
Arabidopsis
phloem
protophloem
receptor kinase
secondary growth
vasculature
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
29
01
2023
accepted:
13
04
2023
medline:
30
6
2023
pubmed:
27
5
2023
entrez:
27
5
2023
Statut:
ppublish
Résumé
The evolution of the plant vascular system is a key process in Earth history because it enabled plants to conquer land and transform the terrestrial surface. Among the vascular tissues, the phloem is particularly intriguing because of its complex functionality. In angiosperms, its principal components are the sieve elements, which transport phloem sap, and their neighboring companion cells. Together, they form a functional unit that sustains sap loading, transport, and unloading. The developmental trajectory of sieve elements is unique among plant cell types because it entails selective organelle degradation including enucleation. Meticulous analyses of primary, so-called protophloem in the Arabidopsis thaliana root meristem have revealed key steps in protophloem sieve element formation at single-cell resolution. A transcription factor cascade connects specification with differentiation and also orchestrates phloem pole patterning via noncell-autonomous action of sieve element-derived effectors. Reminiscent of vascular tissue patterning in secondary growth, these involve receptor kinase pathways, whose antagonists guide the progression of sieve element differentiation. Receptor kinase pathways may also safeguard phloem formation by maintaining the developmental plasticity of neighboring cell files. Our current understanding of protophloem development in the A. thaliana root has reached sufficient detail to instruct molecular-level investigation of phloem formation in other organs.
Substances chimiques
Arabidopsis Proteins
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
852-867Informations de copyright
© 2023 The Author. New Phytologist © 2023 New Phytologist Foundation.
Références
Abrash EB, Davies KA, Bergmann DC. 2011. Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand-receptor interactions. Plant Cell 23: 2864-2879.
Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. 2011. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genetics 7: e1001312.
Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B. 2004. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120.
Aliaga Fandino AC, Hardtke CS. 2022. Auxin transport in developing protophloem: a case study in canalization. Journal of Plant Physiology 269: 153594.
Anne P, Amiguet-Vercher A, Brandt B, Kalmbach L, Geldner N, Hothorn M, Hardtke CS. 2018. CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis. Development 145: dev162354.
Anne P, Azzopardi M, Gissot L, Beaubiat S, Hematy K, Palauqui JC. 2015. OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Current Biology 25: 2584-2590.
Anne P, Hardtke CS. 2017. Phloem function and development-biophysics meets genetics. Current Opinion in Plant Biology 43: 22-28.
Bagdassarian KS, Brown CM, Jones ET, Etchells P. 2020. Connections in the cambium, receptors in the ring. Current Opinion in Plant Biology 57: 96-103.
Barbosa IC, Shikata H, Zourelidou M, Heilmann M, Heilmann I, Schwechheimer C. 2016. Phospholipid composition and a polybasic motif determine D6 PROTEIN KINASE polar association with the plasma membrane and tropic responses. Development 143: 4687-4700.
Barratt DH, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM. 2011. Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiology 155: 328-341.
Beerling DJ. 2007. The emerald planet: how plants changed Earth's history. Oxford, UK; New York, NY, USA: Oxford University Press.
Berckmans B, Kirschner G, Gerlitz N, Stadler R, Simon R. 2020. CLE40 signaling regulates root stem cell fate. Plant Physiology 182: 1776-1792.
van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B. 1995. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378: 62-65.
Berleth T, Mattsson J, Hardtke CS. 2000. Vascular continuity and auxin signals. Trends in Plant Science 5: 387-393.
Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benkova E, Mahonen AP, Helariutta Y. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Current Biology 21: 917-926.
Blumke P, Schlegel J, Gonzalez-Ferrer C, Becher S, Pinto KG, Monaghan J, Simon R. 2021. Receptor-like cytoplasmic kinase MAZZA mediates developmental processes with CLAVATA1 family receptors in Arabidopsis. Journal of Experimental Botany 72: 4853-4870.
Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y. 2003. APL regulates vascular tissue identity in Arabidopsis. Nature 426: 181-186.
Breda AS, Hazak O, Hardtke CS. 2017. Phosphosite charge rather than shootward localization determines OCTOPUS activity in root protophloem. Proceedings of the National Academy of Sciences, USA 114: E5721-E5730.
Breda AS, Hazak O, Schultz P, Anne P, Graeff M, Simon R, Hardtke CS. 2019. A cellular insulator against CLE45 peptide signaling. Current Biology 29: 2501-2508.
Brodribb TJ, Carriqui M, Delzon S, McAdam SAM, Holbrook NM. 2020. Advanced vascular function discovered in a widespread moss. Nature Plants 6: 273-279.
Cattaneo P, Graeff M, Marhava P, Hardtke CS. 2019. Conditional effects of the epigenetic regulator JUMONJI 14 in Arabidopsis root growth. Development 146: dev183905.
Cattaneo P, Hardtke CS. 2017. BIG BROTHER uncouples cell proliferation from elongation in the Arabidopsis primary root. Plant & Cell Physiology 58: 1519-1527.
Chaffey N, Cholewa E, Regan S, Sundberg B. 2002. Secondary xylem development in Arabidopsis: a model for wood formation. Physiologia Plantarum 114: 594-600.
Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335: 207-211.
Chen Q, Soulay F, Saudemont B, Elmayan T, Marmagne A, Masclaux-Daubresse CL. 2019. Overexpression of ATG8 in Arabidopsis stimulates autophagic activity and increases nitrogen remobilization efficiency and grain filling. Plant & Cell Physiology 60: 343-352.
Cho H, Cho HS, Nam H, Jo H, Yoon J, Park C, Dang TVT, Kim E, Jeong J, Park S et al. 2018. Translational control of phloem development by RNA G-quadruplex-JULGI determines plant sink strength. Nature Plants 4: 376-390.
Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett MJ et al. 2014. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nature Cell Biology 16: 66-76.
Clay NK, Nelson T. 2002. VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell 14: 2707-2722.
Crook AD, Willoughby AC, Hazak O, Okuda S, VanDerMolen KR, Soyars CL, Cattaneo P, Clark NM, Sozzani R, Hothorn M et al. 2020. BAM1/2 receptor kinase signaling drives CLE peptide-mediated formative cell divisions in Arabidopsis roots. Proceedings of the National Academy of Sciences, USA 117: 32750-32756.
Czyzewicz N, Wildhagen M, Cattaneo P, Stahl Y, Pinto KG, Aalen RB, Butenko MA, Simon R, Hardtke CS, De Smet I. 2015. Antagonistic peptide technology for functional dissection of CLE peptides revisited. Journal of Experimental Botany 66: 5367-5374.
De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME, Novak O, Yamaguchi N, Yoshida S, Van Isterdael G, Palovaara J et al. 2014. Plant development. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345: 1255215.
De Rybel B, Audenaert D, Vert G, Rozhon W, Mayerhofer J, Peelman F, Coutuer S, Denayer T, Jansen L, Nguyen L et al. 2009. Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling. Chemistry & Biology 16: 594-604.
De Rybel B, Moller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith RS, Borst JW, Weijers D. 2013. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Developmental Cell 24: 426-437.
DeFalco TA, Anne P, James SR, Willoughby AC, Schwanke F, Johanndrees O, Genolet Y, Derbyshire P, Wang Q, Rana S et al. 2022. A conserved module regulates receptor kinase signalling in immunity and development. Nature Plants 8: 356-365.
Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS. 2013. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proceedings of the National Academy of Sciences, USA 110: 7074-7079.
Diaz-Ardila HN, Gujas B, Wang Q, Moret B, Hardtke CS. 2023. pH-dependent CLE peptide perception permits phloem differentiation in Arabidopsis roots. Current Biology 33: 597-605.
Du M, Spalding EP, Gray WM. 2020. Rapid auxin-mediated cell expansion. Annual Review of Plant Biology 71: 379-402.
El-Showk S, Help-Rinta-Rahko H, Blomster T, Siligato R, Maree AF, Mahonen AP, Grieneisen VA. 2015. Parsimonious model of vascular patterning links transverse hormone fluxes to lateral root initiation: auxin leads the way, while cytokinin levels out. PLoS Computational Biology 11: e1004450.
Endo S, Iwai Y, Fukuda H. 2019. Cargo-dependent and cell wall-associated xylem transport in Arabidopsis. New Phytologist 222: 159-170.
Esau K. 1977. Anatomy of seed plants. New York, NY, USA: John Wiley & Sons.
Etchells JP, Provost CM, Mishra L, Turner SR. 2013. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140: 2224-2234.
Fabregas N, Lozano-Elena F, Blasco-Escamez D, Tohge T, Martinez-Andujar C, Albacete A, Osorio S, Bustamante M, Riechmann JL, Nomura T et al. 2018. Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth. Nature Communications 9: 4680.
Fisher K, Turner S. 2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Current Biology 17: 1061-1066.
Fujiwara M, Imamura M, Matsushita K, Roszak P, Yamashino T, Hosokawa Y, Nakajima K, Fujimoto K, Miyashima S. 2023. Patterned proliferation orients tissue-wide stress to control root vascular symmetry in Arabidopsis. Current Biology 33: 886-898.
Fukuda H. 1997. Tracheary element differentiation. Plant Cell 9: 1147-1156.
Fukuda H. 2000. Programmed cell death of tracheary elements as a paradigm in plants. Plant Molecular Biology 44: 245-253.
Fukuda H, Hardtke CS. 2020. Peptide signaling pathways in vascular differentiation. Plant Physiology 182: 1636-1644.
Fukuda H, Ohashi-Ito K. 2019. Vascular tissue development in plants. Current Topics in Developmental Biology 131: 141-160.
Furuta KM, Hellmann E, Helariutta Y. 2014a. Molecular control of cell specification and cell differentiation during procambial development. Annual Review of Plant Biology 65: 607-638.
Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo JO, Vaten A, Lindgren O, De Rybel B, Van Isterdael G et al. 2014b. Plant development. Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345: 933-937.
Graeff M, Hardtke CS. 2021. Metaphloem development in the Arabidopsis root tip. Development 148: dev199766.
Graeff M, Rana S, Marhava P, Moret B, Hardtke CS. 2020. Local and systemic effects of Brassinosteroid perception in developing phloem. Current Biology 30: 1626-1638.
Gray JW, Nelson Dittrich AC, Chen S, Avila J, Giavalisco P, Devarenne TP. 2013. Two Pdk1 phosphorylation sites on the plant cell death suppressor Adi3 contribute to substrate phosphorylation. Biochimica et Biophysica Acta 1834: 1099-1106.
Gujas B, Kastanaki E, Sturchler A, Cruz TMD, Ruiz-Sola MA, Dreos R, Eicke S, Truernit E, Rodriguez-Villalon A. 2020. A reservoir of pluripotent phloem cells safeguards the linear developmental trajectory of protophloem sieve elements. Current Biology 30: 755-766.
Gursanscky NR, Jouannet V, Grunwald K, Sanchez P, Laaber-Schwarz M, Greb T. 2016. MOL1 is required for cambium homeostasis in Arabidopsis. The Plant Journal 86: 210-220.
Hajny J, Tan S, Friml J. 2022. Auxin canalization: from speculative models toward molecular players. Current Opinion in Plant Biology 65: 102174.
Han S, Cho H, Noh J, Qi J, Jung HJ, Nam H, Lee S, Hwang D, Greb T, Hwang I. 2018. BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth. Nature Plants 4: 605-614.
Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez-Villalon A, Hothorn M, Hardtke CS. 2017. Perception of root-active CLE peptides requires CORYNE function in the phloem vasculature. EMBO Reports 18: 1367-1381.
Heo JO, Blob B, Helariutta Y. 2017. Differentiation of conductive cells: a matter of life and death. Current Opinion in Plant Biology 35: 23-29.
Hirakawa Y, Kondo Y, Fukuda H. 2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22: 2618-2629.
Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H. 2008. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proceedings of the National Academy of Sciences, USA 105: 15208-15213.
Hu C, Zhu Y, Cui Y, Zeng L, Li S, Meng F, Huang S, Wang W, Kui H, Yi J et al. 2022. A CLE-BAM-CIK signalling module controls root protophloem differentiation in Arabidopsis. New Phytologist 233: 282-296.
Ibanes M, Fabregas N, Chory J, Cano-Delgado AI. 2009. Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proceedings of the National Academy of Sciences, USA 106: 13630-13635.
Ikematsu S, Tasaka M, Torii KU, Uchida N. 2017. ERECTA-family receptor kinase genes redundantly prevent premature progression of secondary growth in the Arabidopsis hypocotyl. New Phytologist 213: 1697-1709.
Ingram P, Dettmer J, Helariutta Y, Malamy JE. 2011. Arabidopsis lateral root development 3 is essential for early phloem development and function, and hence for normal root system development. The Plant Journal 68: 455-467.
Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842-845.
Kalmbach L, Helariutta Y. 2019. Sieve plate pores in the phloem and the unknowns of their formation. Plants 8: 25.
Kang J, Wang X, Ishida T, Grienenberger E, Zheng Q, Wang J, Zhang Y, Chen W, Chen M, Song XF et al. 2022. A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana. New Phytologist 235: 2300-2312.
Kang YH, Breda A, Hardtke CS. 2017. Brassinosteroid signaling directs formative cell divisions and protophloem differentiation in Arabidopsis root meristems. Development 144: 272-280.
Kang YH, Hardtke CS. 2016. Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling. EMBO Reports 17: 1145-1154.
Kim H, Zhou J, Kumar D, Jang G, Ryu KH, Sebastian J, Miyashima S, Helariutta Y, Lee JY. 2020. SHORTROOT-mediated intercellular signals coordinate phloem development in Arabidopsis roots. Plant Cell 32: 1519-1535.
Kim JY, Symeonidi E, Pang TY, Denyer T, Weidauer D, Bezrutczyk M, Miras M, Zollner N, Hartwig T, Wudick MM et al. 2021. Distinct identities of leaf phloem cells revealed by single cell transcriptomics. Plant Cell 33: 511-530.
Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S. 2007. Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant & Cell Physiology 48: 1821-1825.
Kneuper I, Teale W, Dawson JE, Tsugeki R, Katifori E, Palme K, Ditengou FA. 2021. Auxin biosynthesis and cellular efflux act together to regulate leaf vein patterning. Journal of Experimental Botany 72: 1151-1165.
Knoblauch M, Knoblauch J, Mullendore DL, Savage JA, Babst BA, Beecher SD, Dodgen AC, Jensen KH, Holbrook NM. 2016. Testing the Munch hypothesis of long distance phloem transport in plants. eLife 5: e15341.
Knoblauch M, Oparka K. 2012. The structure of the phloem - still more questions than answers. The Plant Journal 70: 147-156.
Knoblauch M, van Bel AJE. 1998. Sieve tubes in action. Plant Cell 10: 35-50.
Koh SWH, Marhava P, Rana S, Graf A, Moret B, Bassukas AEL, Zourelidou M, Kolb M, Hammes UZ, Schwechheimer C et al. 2021. Mapping and engineering of auxin-induced plasma membrane dissociation in BRX family proteins. Plant Cell 33: 1945-1960.
Kondo Y, Fujita T, Sugiyama M, Fukuda H. 2015. A novel system for xylem cell differentiation in Arabidopsis thaliana. Molecular Plant 8: 612-621.
Kondo Y, Ito T, Nakagami H, Hirakawa Y, Saito M, Tamaki T, Shirasu K, Fukuda H. 2014. Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling. Nature Communications 5: 3504.
Kondo Y, Nurani AM, Saito C, Ichihashi Y, Saito M, Yamazaki K, Mitsuda N, Ohme-Takagi M, Fukuda H. 2016. Vascular cell induction culture system using arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element-like cells. Plant Cell 28: 1250-1262.
Kurihara D, Mizuta Y, Sato Y, Higashiyama T. 2015. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142: 4168-4179.
Lehmann F, Hardtke CS. 2016. Secondary growth of the Arabidopsis hypocotyl-vascular development in dimensions. Current Opinion in Plant Biology 29: 9-15.
Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez L, Merrin J, Chen J, Shabala L, Smet W, Ren H et al. 2021. Cell surface and intracellular auxin signalling for H(+) fluxes in root growth. Nature 599: 273-277.
Liebsch D, Sunaryo W, Holmlund M, Norberg M, Zhang J, Hall HC, Helizon H, Jin X, Helariutta Y, Nilsson O et al. 2014. Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development 141: 4311-4319.
Lopez-Salmeron V, Cho H, Tonn N, Greb T. 2019. The phloem as a mediator of plant growth plasticity. Current Biology 29: R173-R181.
Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y. 2000. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes & Development 14: 2938-2943.
Mahonen AP, Ten Tusscher K, Siligato R, Smetana O, Diaz-Trivino S, Salojarvi J, Wachsman G, Prasad K, Heidstra R, Scheres B. 2014. PLETHORA gradient formation mechanism separates auxin responses. Nature 515: 125-129.
Makila R, Wybouw B, Smetana O, Vainio L, Sole-Gil A, Lyu M, Ye L, Wang X, Siligato R, Jenness MK et al. 2023. Gibberellins promote polar auxin transport to regulate stem cell fate decisions in cambium. Nature Plants 9: 631-644.
Marhava P, Aliaga Fandino AC, Koh SWH, Jelinkova A, Kolb M, Janacek DP, Breda AS, Cattaneo P, Hammes UZ, Petrasek J et al. 2020. Plasma membrane domain patterning and self-reinforcing polarity in Arabidopsis. Developmental Cell 52: 223-235.
Marhava P, Bassukas AEL, Zourelidou M, Kolb M, Moret B, Fastner A, Schulze WX, Cattaneo P, Hammes UZ, Schwechheimer C et al. 2018. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature 558: 297-300.
Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo JO, Mellor N, Help-Rinta-Rahko H, Otero S, Smet W et al. 2019. Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature 565: 490-494.
Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K. 2007. Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. The Plant Journal 50: 751-766.
Moret B, Marhava P, Aliaga Fandino AC, Hardtke CS, Ten Tusscher KHW. 2020. Local auxin competition explains fragmented differentiation patterns. Nature Communications 11: 2965.
Mouchel CF, Briggs GC, Hardtke CS. 2004. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes & Development 18: 700-714.
Nimchuk ZL. 2017. CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop. PLoS Genetics 13: e1006681.
Nodine MD, Yadegari R, Tax FE. 2007. RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Developmental Cell 12: 943-956.
Otero S, Gildea I, Roszak P, Lu Y, Di Vittori V, Bourdon M, Kalmbach L, Blob B, Heo JO, Peruzzo F et al. 2022. A root phloem pole cell atlas reveals common transcriptional states in protophloem-adjacent cells. Nature Plants 8: 954-970.
Peng Y, Ma W, Chen L, Yang L, Li S, Zhao H, Zhao Y, Jin W, Li N, Bevan MW et al. 2013. Control of root meristem size by DA1-RELATED PROTEIN2 in Arabidopsis. Plant Physiology 161: 1542-1556.
Pratt RB, Jacobsen AL. 2017. Conflicting demands on angiosperm xylem: tradeoffs among storage, transport and biomechanics. Plant, Cell & Environment 40: 897-913.
Qian P, Song W, Yokoo T, Minobe A, Wang G, Ishida T, Sawa S, Chai J, Kakimoto T. 2018. The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors. Nature Plants 4: 1071-1081.
Qian P, Song W, Zaizen-Iida M, Kume S, Wang G, Zhang Y, Kinoshita-Tsujimura K, Chai J, Kakimoto T. 2022. A Dof-CLE circuit controls phloem organization. Nature Plants 8: 817-827.
Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS. 2011. Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23: 1322-1336.
Raven JA. 2003. Long-distance transport in non-vascular plants. Plant, Cell & Environment 26: 73-85.
Ravichandran SJ, Linh NM, Scarpella E. 2020. The canalization hypothesis - challenges and alternatives. New Phytologist 227: 1051-1059.
Ren SC, Song XF, Chen WQ, Lu R, Lucas WJ, Liu CM. 2019. CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex. Journal of Integrative Plant Biology 61: 1043-1061.
Riesmeier JW, Hirner B, Frommer WB. 1993. Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5: 1591-1598.
Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P, Depuydt S, Hardtke CS. 2014. Molecular genetic framework for protophloem formation. Proceedings of the National Academy of Sciences, USA 111: 11551-11556.
Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS. 2015. Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development 142: 1437-1446.
Roschzttardtz H, Paez-Valencia J, Dittakavi T, Jali S, Reyes FC, Baisa G, Anne P, Gissot L, Palauqui JC, Masson PH et al. 2014. The VASCULATURE COMPLEXITY AND CONNECTIVITY gene encodes a plant-specific protein required for embryo provasculature development. Plant Physiology 166: 889-902.
Ross-Elliott TJ, Jensen KH, Haaning KS, Wager BM, Knoblauch J, Howell AH, Mullendore DL, Monteith AG, Paultre D, Yan D et al. 2017. Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife 6: e24125.
Roszak P, Heo JO, Blob B, Toyokura K, Sugiyama Y, de Luis Balaguer MA, Lau WWY, Hamey F, Cirrone J, Madej E et al. 2021. Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization. Science 374: eaba5531.
Ruiz Sola MA, Coiro M, Crivelli S, Zeeman SC, Schmidt Kjolner Hansen S, Truernit E. 2017. OCTOPUS-LIKE 2, a novel player in Arabidopsis root and vascular development, reveals a key role for OCTOPUS family genes in root metaphloem sieve tube differentiation. New Phytologist 216: 1191-1204.
Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P et al. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463-472.
Sankar M, Nieminen K, Ragni L, Xenarios I, Hardtke CS. 2014. Automated quantitative histology reveals vascular morphodynamics during Arabidopsis hypocotyl secondary growth. eLife 3: e01567.
Santuari L, Sanchez-Perez GF, Luijten M, Rutjens B, Terpstra I, Berke L, Gorte M, Prasad K, Bao D, Timmermans-Hereijgers JL et al. 2016. The PLETHORA gene regulatory network guides growth and cell differentiation in Arabidopsis roots. Plant Cell 28: 2937-2951.
Santuari L, Scacchi E, Rodriguez-Villalon A, Salinas P, Dohmann EM, Brunoud G, Vernoux T, Smith RS, Hardtke CS. 2011. Positional information by differential endocytosis splits auxin response to drive Arabidopsis root meristem growth. Current Biology 21: 1918-1923.
Serra O, Mahonen AP, Hetherington AJ, Ragni L. 2022. The making of plant armor: the periderm. Annual Review of Plant Biology 73: 405-432.
Shi D, Lebovka I, Lopez-Salmeron V, Sanchez P, Greb T. 2019. Bifacial cambium stem cells generate xylem and phloem during radial plant growth. Development 146: dev171355.
Sibout R, Plantegenet S, Hardtke CS. 2008. Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Current Biology 18: 458-463.
Slupianek A, Dolzblasz A, Sokolowska K. 2021. Xylem parenchyma-role and relevance in wood functioning in trees. Plants 10: 1247.
Smetana O, Makila R, Lyu M, Amiryousefi A, Sanchez Rodriguez F, Wu MF, Sole-Gil A, Leal Gavarron M, Siligato R, Miyashima S et al. 2019. High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565: 485-489.
Smit ME, McGregor SR, Sun H, Gough C, Bagman AM, Soyars CL, Kroon JT, Gaudinier A, Williams CJ, Yang X et al. 2020. A PXY-mediated transcriptional network integrates signaling mechanisms to control vascular development in Arabidopsis. Plant Cell 32: 319-335.
Spencer V, Nemec Venza Z, Harrison CJ. 2021. What can lycophytes teach us about plant evolution and development? Modern perspectives on an ancient lineage. Evolution & Development 23: 174-196.
Spicer R, Groover A. 2010. Evolution of development of vascular cambia and secondary growth. New Phytologist 186: 577-592.
Suer S, Agusti J, Sanchez P, Schwarz M, Greb T. 2011. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23: 3247-3259.
Tamaki T, Oya S, Naito M, Ozawa Y, Furuya T, Saito M, Sato M, Wakazaki M, Toyooka K, Fukuda H et al. 2020. VISUAL-CC system uncovers the role of GSK3 as an orchestrator of vascular cell type ratio in plants. Communications Biology 3: 184.
Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H, Heilmann M, van Wijk R, Vermeer JE, Heilmann I, Munnik T et al. 2014. Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26: 2114-2128.
Truernit E, Bauby H, Belcram K, Barthelemy J, Palauqui JC. 2012. OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139: 1306-1315.
Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, Palauqui JC. 2008. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20: 1494-1503.
Uchida N, Lee JS, Horst RJ, Lai HH, Kajita R, Kakimoto T, Tasaka M, Torii KU. 2012. Regulation of inflorescence architecture by intertissue layer ligand-receptor communication between endodermis and phloem. Proceedings of the National Academy of Sciences, USA 109: 6337-6342.
Uchida N, Tasaka M. 2013. Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases. Journal of Experimental Botany 64: 5335-5343.
Wallner ES, Lopez-Salmeron V, Belevich I, Poschet G, Jung I, Grunwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y et al. 2017. Strigolactone- and Karrikin-independent SMXL proteins are central regulators of phloem formation. Current Biology 27: 1241-1247.
Wallner ES, Tonn N, Shi D, Jouannet V, Greb T. 2020. SUPPRESSOR OF MAX2 1-LIKE 5 promotes secondary phloem formation during radial stem growth. The Plant Journal 102: 903-915.
Wang N, Bagdassarian KS, Doherty RE, Kroon JT, Connor KA, Wang XY, Wang W, Jermyn IH, Turner SR, Etchells JP. 2019. Organ-specific genetic interactions between paralogues of the PXY and ER receptor kinases enforce radial patterning in Arabidopsis vascular tissue. Development 146: dev177105.
Wang Q, Aliaga Fandino AC, Graeff M, DeFalco TA, Zipfel C, Hardtke CS. 2023. A phosphoinositide hub connects CLE peptide signaling and polar auxin efflux regulation. Nature Communications 14: 423.
Wang W, Hu C, Li X, Zhu Y, Tao L, Cui Y, Deng D, Fan X, Zhang H, Li J et al. 2022. Receptor-like cytoplasmic kinases PBL34/35/36 are required for CLE peptide-mediated signaling to maintain shoot apical meristem and root apical meristem homeostasis in Arabidopsis. Plant Cell 34: 1289-1307.
Wilson-Sanchez D, Martinez-Lopez S, Navarro-Cartagena S, Jover-Gil S, Micol JL. 2018. Members of the DEAL subfamily of the DUF1218 gene family are required for bilateral symmetry but not for dorsoventrality in Arabidopsis leaves. New Phytologist 217: 1307-1321.
Xiao Y, Offringa R. 2020. PDK1 regulates auxin transport and Arabidopsis vascular development through AGC1 kinase PAX. Nature Plants 6: 544-555.
Xie B, Wang X, Zhu M, Zhang Z, Hong Z. 2011. CalS7 encodes a callose synthase responsible for callose deposition in the phloem. The Plant Journal 65: 1-14.
Yanagisawa M, Poitout A, Otegui MS. 2021. Arabidopsis vascular complexity and connectivity controls PIN-FORMED1 dynamics and lateral vein patterning during embryogenesis. Development 148: dev197210.
Zegzouti H, Li W, Lorenz TC, Xie M, Payne CT, Smith K, Glenny S, Payne GS, Christensen SK. 2006. Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. The Journal of Biological Chemistry 281: 35520-35530.
Zhang C, Turgeon R. 2018. Mechanisms of phloem loading. Current Opinion in Plant Biology 43: 71-75.
Zhang H, Lin X, Han Z, Qu LJ, Chai J. 2016. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Research 26: 543-555.
Zourelidou M, Absmanner B, Weller B, Barbosa IC, Willige BC, Fastner A, Streit V, Port SA, Colcombet J, De la Fuente van Bentem S et al. 2014. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3: e02860.