1932

Abstract

Amphibious plants can grow and survive in both aquatic and terrestrial environments. This review explores the diverse adaptations that enable them to thrive in such contrasting habitats. Plants with amphibious lifestyles possess fascinating traits, and their phenotypic plasticity plays an important role in adaptations. Heterophylly, the ability to produce different leaf forms, is one such trait, with submerged leaves generally being longer, narrower, and thinner than aerial leaves. In addition to drastic changes in leaf contours, amphibious plants display significant anatomical and physiological changes, including a reduction in stomatal number and cuticle thickness and changes in photosynthesis mode. This review summarizes and compares the regulatory mechanisms and evolutionary origins of amphibious plants based on molecular biology studies actively conducted in recent years using novel model amphibious plant species. Studying amphibious plants will enhance our understanding of plant adaptations to aquatic environments.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-062923-024919
2024-07-22
2025-02-07
Loading full text...

Full text loading...

/deliver/fulltext/arplant/75/1/annurev-arplant-062923-024919.html?itemId=/content/journals/10.1146/annurev-arplant-062923-024919&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Akman M, Bhikharie A, Mustroph A, Sasidharan R. 2014.. Extreme flooding tolerance in Rorippa. . Plant Signal. Behav. 9::e27847
    [Crossref] [Google Scholar]
  2. 2.
    Alpert P, Simms EL. 2002.. The relative advantages of plasticity and fixity in different environments: When is it good for a plant to adjust?. Evol. Ecol. 16::28597
    [Crossref] [Google Scholar]
  3. 3.
    Althoff F, Wegner L, Ehlers K, Buschmann H, Zachgo S. 2022.. Developmental plasticity of the amphibious liverwort. . Front. Plant Sci. 13::909327
    [Crossref] [Google Scholar]
  4. 4.
    Amano R, Nakayama H, Momoi R, Omata E, Gunji S, et al. 2020.. Molecular basis for natural vegetative propagation via regeneration in North American lake cress, Rorippa aquatica (Brassicaceae). . Plant Cell Physiol. 61::35369
    [Crossref] [Google Scholar]
  5. 5.
    Arber A. 1920.. Water Plants: A Study of Aquatic Angiosperms. Cambridge:: Cambridge Univ. Press
    [Google Scholar]
  6. 6.
    Barret SCH, Graham SW. 1997.. Adaptive radiation in the aquatic plant family Pontederiaceae: insights from phylogenetic analysis. . In Molecular Evolution and Adaptive Radiation, ed. TJ Givnish, KJ Sytsma , pp. 22558. Cambridge:: Cambridge Univ. Press
    [Google Scholar]
  7. 7.
    Barton MK. 2010.. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. . Dev. Biol. 341::95113
    [Crossref] [Google Scholar]
  8. 8.
    Bowles AMC, Paps J, Bechtold U. 2022.. Water-related innovations in land plants evolved by different patterns of gene cooption and novelty. . New Phytol. 235::73242
    [Crossref] [Google Scholar]
  9. 9.
    Bradshaw AD. 1965.. Evolutionary significance of phenotypic plasticity in plants. . Adv. Genet. 13::11555
    [Crossref] [Google Scholar]
  10. 10.
    Braendle R, Crawford RMM. 1999.. Plants as amphibians. . Perspect. Plant Ecol. Evol. Syst. 2::5678
    [Crossref] [Google Scholar]
  11. 11.
    Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C. 2018.. Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. . Plant Physiol. 176::1694708
    [Crossref] [Google Scholar]
  12. 12.
    Burko Y, Willige BC, Seluzicki A, Novák O, Ljung K, Chory J. 2022.. PIF7 is a master regulator of thermomorphogenesis in shade. . Nat. Commun. 13::4942
    [Crossref] [Google Scholar]
  13. 13.
    Casati P, Lara MaV, Andreo CS. 2000.. Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submersed aquatic species. . Plant Physiol. 123::161122
    [Crossref] [Google Scholar]
  14. 14.
    Chen L-Y, Lu B, Morales-Briones DF, Moody ML, Liu F, et al. 2022.. Phylogenomic analyses of Alismatales shed light into adaptations to aquatic environments. . Mol. Biol. Evol. 39::msac079
    [Crossref] [Google Scholar]
  15. 15.
    Chitwood DH, Sinha NR. 2016.. Evolutionary and environmental forces sculpting leaf development. . Curr. Biol. 26::297306
    [Crossref] [Google Scholar]
  16. 16.
    Colmer TD, Winkel A, Pedersen O. 2011.. A perspective on underwater photosynthesis in submerged terrestrial wetland plants. . AoB PLANTS 2011::plr030
    [Crossref] [Google Scholar]
  17. 17.
    Cook CDK. 1999.. The number and kinds of embryo-bearing plants which have become aquatic: a survey. . Perspect. Plant Ecol. Evol. Syst. 2::79102
    [Crossref] [Google Scholar]
  18. 18.
    Cook SA, Johnson MP. 1968.. Adaptation to heterogenous environments. I. Variation in heterophylly in Ranunculus flammura L. . Evolution 22::496516
    [Google Scholar]
  19. 19.
    Crawford RMM. 1987.. Plant Life in Aquatic and Amphibious Habitats. Edinburgh:: Blackwell Sci. Publ.
    [Google Scholar]
  20. 20.
    Donoghue PCJ, Harrison CJ, Paps J, Schneider H. 2021.. The evolutionary emergence of land plants. . Curr. Biol. 31::128198
    [Crossref] [Google Scholar]
  21. 21.
    Du F, Guan C, Jiao Y. 2018.. Molecular mechanisms of leaf morphogenesis. . Mol. Plant 11::111734
    [Crossref] [Google Scholar]
  22. 22.
    Du ZY, Wang QF. 2014.. Correlations of life form, pollination mode and sexual system in aquatic angiosperms. . PLOS ONE 9::e115653
    [Crossref] [Google Scholar]
  23. 23.
    Du ZY, Wang QF, China Phylogeny Consort. 2016.. Phylogenetic tree of vascular plants reveals the origins of aquatic angiosperms. . J. Syst. Evol. 54::34248
    [Crossref] [Google Scholar]
  24. 24.
    Dubois M, Van den Broeck L, Inzé D. 2018.. The pivotal role of ethylene in plant growth. . Trends Plant Sci. 23::31123
    [Crossref] [Google Scholar]
  25. 25.
    Dupree P, Pwee KH, Gray JC. 1991.. Expression of photosynthesis gene-promoter fusions in leaf epidermal cells of transgenic tobacco plants. . Plant J. 1::11520
    [Crossref] [Google Scholar]
  26. 26.
    Efroni I, Blum E, Goldshmidt A, Eshed Y. 2008.. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. . Plant Cell 20::2293306
    [Crossref] [Google Scholar]
  27. 27.
    Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, et al. 2003.. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. . Curr. Biol. 13::176874
    [Crossref] [Google Scholar]
  28. 28.
    Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, et al. 2006.. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. . Curr. Biol. 16::93944
    [Crossref] [Google Scholar]
  29. 29.
    Frost-Christensen H, Jørgensen BL, Floto F. 2003.. Species specificity of resistance to oxygen diffusion in thin cuticular membranes from amphibious plants. . Plant Cell Environ. 26::56169
    [Crossref] [Google Scholar]
  30. 30.
    Frost-Christensen H, Sand-Jensen K. 1995.. Comparative kinetics of photosynthesis in floating and submerged Potamogeton leaves. . Aquat. Bot. 51::12134
    [Crossref] [Google Scholar]
  31. 31.
    Goliber TE, Feldman LJ. 1990.. Developmental analysis of leaf plasticity in the heterophyllous aquatic plant Hippuris vulgaris. . Am. J. Bot. 77::399412
    [Crossref] [Google Scholar]
  32. 32.
    Grace JB. 1993.. The adaptive significance of clonal reproduction in angiosperms: an aquatic perspective. . Aquat. Bot. 44::15980
    [Crossref] [Google Scholar]
  33. 33.
    Gross EM, Groffier H, Pestelard C, Hussner A. 2020.. Ecology and environmental impact of Myriophyllum heterophyllum, an aggressive invader in European waterways. . Diversity 12::127
    [Crossref] [Google Scholar]
  34. 34.
    Guo M, Thomas J, Collins G, Timmermans MC. 2008.. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. . Plant Cell 20::4858
    [Crossref] [Google Scholar]
  35. 35.
    Han S, Xing Z, Jiang H, Li W, Huang W. 2021.. Biological adaptive mechanisms displayed by a freshwater plant to live in aquatic and terrestrial environments. . Environ. Exp. Bot. 191::104623
    [Crossref] [Google Scholar]
  36. 36.
    Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 2007.. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. . Genes Dev. 21::172025
    [Crossref] [Google Scholar]
  37. 37.
    Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, et al. 2009.. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. . Plant Cell Physiol. 50::101931
    [Crossref] [Google Scholar]
  38. 38.
    Harada D, Yamato KT, Izui K, Akita M. 2018.. De novo short read assembly and functional annotation of Eleocharis vivipara, a C3/C4 interconvertible sedge plant. . Environ. Control Biol. 56::8187
    [Crossref] [Google Scholar]
  39. 39.
    Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. 1996.. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. . Cell 84::73544
    [Crossref] [Google Scholar]
  40. 40.
    Hattori Y, Nagai K, Furukawa S, Song X-J, Kawano R, et al. 2009.. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. . Nature 460::102630
    [Crossref] [Google Scholar]
  41. 41.
    Hay A, Barkoulas M, Tsiantis M. 2006.. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. . Development 133::395561
    [Crossref] [Google Scholar]
  42. 42.
    Hay A, Tsiantis M. 2006.. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. . Nat. Genet. 38::94247
    [Crossref] [Google Scholar]
  43. 43.
    Hay A, Tsiantis M. 2010.. KNOX genes: versatile regulators of plant development and diversity. . Development 137::315365
    [Crossref] [Google Scholar]
  44. 44.
    He D, Guo P, Gugger F, Guo Y, Liu X, Chen J. 2018.. Investigating the molecular basis for heterophylly in the aquatic plant Potamogeton octandrus (Potamogetonaceae) with comparative transcriptomics. . PeerJ 6::e4448
    [Crossref] [Google Scholar]
  45. 45.
    Hibara K, Karim MR, Takada S, Taoka K, Furutani M, et al. 2006.. Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. . Plant Cell 18::294657
    [Crossref] [Google Scholar]
  46. 46.
    Hörandl E, Emadzade K. 2012.. Evolutionary classification: a case study on the diverse plant genus Ranunculus L. (Ranunculaceae). . Perspect. Plant Ecol. Evol. Syst. 14::31024
    [Crossref] [Google Scholar]
  47. 47.
    Hörandl E, Paun O, Johansson JT, Lehnebach C, Armstrong T, et al. 2005.. Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. . Mol. Phylogenet. Evol. 36::30527
    [Crossref] [Google Scholar]
  48. 48.
    Horiguchi G, Matsumoto K, Nemoto K, Inokuchi M, Hirotsu N. 2021.. Transition from proto-Kranz-type photosynthesis to HCO3 use photosynthesis in the amphibious plant Hygrophila polysperma. . Front. Plant Sci. 12::675507 48. Indicates that H. polysperma switches the type of photosynthesis it uses between terrestrial and submerged environments.
    [Crossref] [Google Scholar]
  49. 49.
    Horiguchi G, Nemoto K, Yokoyama T, Hirotsu N. 2019.. Photosynthetic acclimation of terrestrial and submerged leaves in the amphibious plant Hygrophila difformis. . AoB PLANTS 11::plz009
    [Crossref] [Google Scholar]
  50. 50.
    Horiguchi G, Oyama R, Akabane T, Suzuki N, Katoh E, et al. 2023.. Cooperation of external carbonic anhydrase and HCO3 transporter supports underwater photosynthesis in submerged leaves of the amphibious plant Hygrophila difformis. . Ann. Bot. 2023::mcad161
    [Google Scholar]
  51. 51.
    Huang W, Han S, Jiang H, Gu S, Li W, et al. 2020.. External α-carbonic anhydrase and solute carrier 4 are required for bicarbonate uptake in a freshwater angiosperm. . J. Exp. Bot. 71::600414
    [Crossref] [Google Scholar]
  52. 52.
    Iida S, Ikeda M, Amano M, Sakayama H, Kadono Y, Kosuge K. 2016.. Loss of heterophylly in aquatic plants: not ABA-mediated stress but exogenous ABA treatment induces stomatal leaves in Potamogeton perfoliatus. . J. Plant Res. 129::85362 52. Suggests that differences in ABA-mediated stress responses between the two Potamogeton species are the cause of heterophylly loss.
    [Crossref] [Google Scholar]
  53. 53.
    Iida S, Miyagi A, Aoki S, Ito M, Kadono Y, Kosuge K. 2009.. Molecular adaptation of rbcL in the heterophyllous aquatic plant Potamogeton. . PLOS ONE 4::e4633
    [Crossref] [Google Scholar]
  54. 54.
    Ikematsu S, Umase T, Shiozaki M, Nakayama S, Noguchi F, et al. 2023.. Rewiring of hormones and light response pathways underlies the inhibition of stomatal development in an amphibious plant Rorippa aquatica underwater. . Curr. Biol. 33::54356 54. Reveals that ethylene and light signaling play central roles in suppressing stomata development upon submergence in Rorippa aquatica.
    [Crossref] [Google Scholar]
  55. 55.
    Irieda H, Takano Y. 2021.. Epidermal chloroplasts are defense-related motile organelles equipped with plant immune components. . Nat. Commun. 12::2739
    [Crossref] [Google Scholar]
  56. 56.
    Ito Y, Tanaka N, Barfod AS, Kaul RB, Muasya AM, et al. 2017.. From terrestrial to aquatic habitats and back again: molecular insights into the evolution and phylogeny of Callitriche (Plantaginaceae). . Bot. J. Linnean Soc. 184::4658
    [Crossref] [Google Scholar]
  57. 57.
    Janssen BJ, Lund L, Sinha N. 1998.. Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. . Plant Physiol. 117::77186
    [Crossref] [Google Scholar]
  58. 58.
    Kadono Y. 2014.. A Field Guide to Aquatic Plants of Japan. Tokyo, Japan:: Bun-ichi Co. Ltd.
    [Google Scholar]
  59. 59.
    Kanaoka MM, Pillitteri L, Fujii H, Yoshida Y, Bogenschutz NL, et al. 2008.. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. . Plant Cell 20::177585
    [Crossref] [Google Scholar]
  60. 60.
    Kazama T, Ichihashi Y, Murata S, Tsukaya H. 2010.. The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. . Plant Cell Physiol. 51::104654
    [Crossref] [Google Scholar]
  61. 61.
    Keeley JE. 1998.. CAM photosynthesis in submerged aquatic plants. . Bot. Rev. 64::12175
    [Crossref] [Google Scholar]
  62. 62.
    Keeley JE. 2014.. Aquatic CAM photosynthesis: a brief history of its discovery. . Aquat. Bot. 118::3844
    [Crossref] [Google Scholar]
  63. 63.
    Keeley JE, Busch G. 1984.. Carbon assimilation characteristics of the aquatic CAM plant, Isoetes howellii.. Plant Physiol. 76::52530 63. Shows that Isoetes howellii conducts CAM photosynthesis in water and C3 photosynthesis on land.
    [Crossref] [Google Scholar]
  64. 64.
    Kidner CA, Timmermans MC. 2010.. Signaling sides adaxial–abaxial patterning in leaves. . Curr. Top. Dev. Biol. 91::14168
    [Crossref] [Google Scholar]
  65. 65.
    Kidner CA, Umbreen S. 2010.. Why is leaf shape so variable?. Int. J. Plant Dev. Biol. 4::6475
    [Google Scholar]
  66. 66.
    Kim J, Joo Y, Kyung J, Jeon M, Park JY, et al. 2018.. A molecular basis behind heterophylly in an amphibious plant, Ranunculus trichophyllus. . PLOS Genet. 14::e1007208 66. Shows a direct link between the submergence response pathway and regulatory mechanisms of leaf development in Ranunculus trichophyllus.
    [Crossref] [Google Scholar]
  67. 67.
    Koga H, Doll Y, Hashimoto K, Toyooka K, Tsukaya H. 2020.. Dimorphic leaf development of the aquatic plant Callitriche palustris L. through differential cell division and expansion. . Front. Plant Sci. 11::269
    [Crossref] [Google Scholar]
  68. 68.
    Koga H, Kojima M, Takebayashi Y, Sakakibara H, Tsukaya H. 2021.. Identification of the unique molecular framework of heterophylly in the amphibious plant Callitriche palustris L. . Plant Cell 33::327292 68. Discovered that the molecular mechanism regulating heterophylly in Callitriche palustris is associated with hormonal changes and expression of various transcription factors.
    [Crossref] [Google Scholar]
  69. 69.
    Koga K, Kadono Y, Setoguchi H. 2008.. Phylogeography of Japanese water crowfoot based on chloroplast DNA haplotypes. . Aquat. Bot. 89::18
    [Crossref] [Google Scholar]
  70. 70.
    Kosma DK, Bourdenx B, Bernard A, Parsons EP, S, et al. 2009.. The impact of water deficiency on leaf cuticle lipids of Arabidopsis. . Plant Physiol. 151::191829
    [Crossref] [Google Scholar]
  71. 71.
    Kozlowski G, Stoffel M, Bétrisey S, Cardinaux L, Mota M. 2015.. Hydrophobia of gymnosperms: myth or reality? A global analysis. . Ecohydrology 8::10512
    [Crossref] [Google Scholar]
  72. 72.
    Kuwabara A, Nagata T. 2006.. Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae). . Planta 224::76170
    [Crossref] [Google Scholar]
  73. 73.
    Lansdown RV, Bazos I, Caria MC, Troia A, Wieringa JJ. 2017.. New distribution and taxonomic information on Callitriche (Plantaginaceae) in the Mediterranean region. . Phytotaxa 313::91104
    [Crossref] [Google Scholar]
  74. 74.
    Les DH. 2018.. Aquatic Dicotyledons of North America: Ecology, Life History, and Systematics. Boca Raton, FL:: CRC Press
    [Google Scholar]
  75. 75.
    Levis NA, Pfennig DW. 2016.. Evaluating ‘plasticity-first’ evolution in nature: key criteria and empirical approaches. . Trends Ecol. Evol. 31::56374
    [Crossref] [Google Scholar]
  76. 76.
    Li G, Hu S, Hou H, Kimura S. 2019.. Heterophylly: phenotypic plasticity of leaf shape in aquatic and amphibious plants. . Plants 8::420
    [Crossref] [Google Scholar]
  77. 77.
    Li G, Hu S, Yang J, Schultz EA, Clarke K, Hou H. 2017.. Water-Wisteria as an ideal plant to study heterophylly in higher aquatic plants. . Plant Cell Rep. 36::122536
    [Crossref] [Google Scholar]
  78. 78.
    Li G, Hu S, Yang J, Zhao X, Kimura S, et al. 2020.. Establishment of an Agrobacterium mediated transformation protocol for the detection of cytokinin in the heterophyllous plant Hygrophila difformis (Acanthaceae). . Plant Cell Rep. 39::73750
    [Crossref] [Google Scholar]
  79. 79.
    Li G, Hu S, Zhao X, Kumar S, Li Y, et al. 2021.. Mechanisms of the morphological plasticity induced by phytohormones and the environment in plants. . Int. J. Mol. Sci. 22::765
    [Crossref] [Google Scholar]
  80. 80.
    Li G, Yang J, Chen Y, Zhao X, Kimura S, et al. 2022.. SHOOT MERISTEMLESS participates in the heterophylly of Hygrophila difformis (Acanthaceae). . Plant Physiol. 190::177791 80. Shows that HdSTM and HdCUC3 are involved in regulating heterophylly in H. difformis.
    [Crossref] [Google Scholar]
  81. 81.
    Long JA, Moan EI, Medford JI, Barton MK. 1996.. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. . Nature 379::6669
    [Crossref] [Google Scholar]
  82. 82.
    Lumbreras A, Navarro G, Pardo C, Molina J. 2011.. Aquatic Ranunculus communities in the northern hemisphere: a global review. . Plant Biosyst. 145::11822
    [Crossref] [Google Scholar]
  83. 83.
    Lusa MG, Boeger MRT, Moço MCdC, Bona C. 2011.. Morpho-anatomical adaptations of Potamogeton polygonus (Potamogetonaceae) to lotic and lentic environments. . Rodriguésia 62::92736
    [Crossref] [Google Scholar]
  84. 84.
    Maberly SC, Madsen TV. 2002.. Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. . Funct. Plant Biol. 29::393405
    [Crossref] [Google Scholar]
  85. 85.
    Maberly SC, Madsen TV. 2002.. Use of bicarbonate ions as a source of carbon in photosynthesis by Callitriche hermaphroditica. . Aquat. Bot. 73::17
    [Crossref] [Google Scholar]
  86. 86.
    MacAlister CA, Ohashi-Ito K, Bergmann DC. 2007.. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. . Nature 445::53740
    [Crossref] [Google Scholar]
  87. 87.
    Madsen TV, Maberly SC. 1991.. Diurnal variation in light and carbon limitation of photosynthesis by two species of submerged freshwater macrophyte with a differential ability to use bicarbonate. . Freshwater Biol. 26::17587
    [Crossref] [Google Scholar]
  88. 88.
    Marchant DB, Chen G, Cai S, Chen F, Schafran P, et al. 2022.. Dynamic genome evolution in a model fern. . Nat. Plants 8::103851
    [Crossref] [Google Scholar]
  89. 89.
    Marchant DB, Sessa EB, Wolf PG, Heo K, Barbazuk WB, et al. 2019.. The C-Fern (Ceratopteris richardii) genome: insights into plant genome evolution with the first partial homosporous fern genome assembly. . Sci. Rep. 9::18181
    [Crossref] [Google Scholar]
  90. 90.
    Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006.. Plant stomata function in innate immunity against bacterial invasion. . Cell 126::96980
    [Crossref] [Google Scholar]
  91. 91.
    Moczek AP, Sultan S, Foster S, Ledón-Rettig C, Dworkin I, et al. 2011.. The role of developmental plasticity in evolutionary innovation. . Proc. R. Soc. B 278::270513
    [Crossref] [Google Scholar]
  92. 92.
    Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJ. 2005.. Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. . Plant Physiol. 139::497508
    [Crossref] [Google Scholar]
  93. 93.
    Mommer L, Visser EJ. 2005.. Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. . Ann. Bot. 96::58189
    [Crossref] [Google Scholar]
  94. 94.
    Momokawa N, Kadono Y, Kudoh H. 2011.. Effects of light quality on leaf morphogenesis of a heterophyllous amphibious plant, Rotala hippuris. . Ann. Bot. 108::1299306
    [Crossref] [Google Scholar]
  95. 95.
    Müller JT, van Veen H, Bartylla MM, Akman M, Pedersen O, et al. 2021.. Keeping the shoot above water—submergence triggers antithetical growth responses in stems and petioles of watercress (Nasturtium officinale). . New Phytol. 229::14055
    [Crossref] [Google Scholar]
  96. 96.
    Nakayama H, Nakayama N, Seiki S, Kojima M, Sakakibara H, et al. 2014.. Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. . Plant Cell 26::473348 96. Reveals that the KNOX-GA gene module is involved in the regulation of temperature-dependent leaf shape change in R. aquatica.
    [Crossref] [Google Scholar]
  97. 97.
    Nakayama H, Sakamoto T, Okegawa Y, Kaminoyama K, Fujie M, et al. 2018.. Comparative transcriptomics with self-organizing map reveals cryptic photosynthetic differences between two accessions of North American Lake cress. . Sci. Rep. 8::3302
    [Crossref] [Google Scholar]
  98. 98.
    Nakayama H, Sinha NR, Kimura S. 2017.. How do plants and phytohormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues. . Front. Plant Sci. 8::1717
    [Crossref] [Google Scholar]
  99. 99.
    Nath U, Crawford BC, Carpenter R, Coen E. 2003.. Genetic control of surface curvature. . Science 299::14047
    [Crossref] [Google Scholar]
  100. 100.
    Nguyen STT, Greaves T, McCurdy DW. 2017.. Heteroblastic development of transfer cells is controlled by the microRNA miR156/SPL module. . Plant Physiol. 173::167691
    [Crossref] [Google Scholar]
  101. 101.
    Nielsen SL. 1993.. A comparison of aerial and submerged photosynthesis in some Danish amphibious plants. . Aquat. Bot. 45::2740
    [Crossref] [Google Scholar]
  102. 102.
    Nijhout HF, Kudla AM, Hazelwood CC. 2020.. Genetic assimilation and accommodation: models and mechanisms. . Curr. Top. Dev. Biol. 141::33769
    [Crossref] [Google Scholar]
  103. 103.
    Ohashi-Ito K, Bergmann DC. 2006.. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. . Plant Cell 18::2493505
    [Crossref] [Google Scholar]
  104. 104.
    Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, et al. 2016.. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. . Nature 530::33135
    [Crossref] [Google Scholar]
  105. 105.
    Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, et al. 2007.. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. . Nat. Genet. 39::78791
    [Crossref] [Google Scholar]
  106. 106.
    Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. 2000.. Mechanisms that control knox gene expression in the Arabidopsis shoot. . Development 127::552332
    [Crossref] [Google Scholar]
  107. 107.
    Pedersen O, Colmer TD, Sand-Jensen K. 2013.. Underwater photosynthesis of submerged plants—recent advances and methods. . Front. Plant Sci. 4::140
    [Crossref] [Google Scholar]
  108. 108.
    Pfennig DW, ed. 2021.. Phenotypic Plasticity & Evolution: Causes, Consequences, Controversies. Boca Raton, FL:: CRC Press
    [Google Scholar]
  109. 109.
    Philbrick CT, Les DH. 2000.. Phylogenetic studies in Callitriche: implications for interpretation of ecological, karyological and pollination system evolution. . Aquat. Bot. 68::12341
    [Crossref] [Google Scholar]
  110. 110.
    Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU. 2007.. Termination of asymmetric cell division and differentiation of stomata. . Nature 445::5015
    [Crossref] [Google Scholar]
  111. 111.
    Poethig RS. 2010.. The past, present, and future of vegetative phase change. . Plant Physiol. 154::54144
    [Crossref] [Google Scholar]
  112. 112.
    Povilus RA, DaCosta JM, Grassa C, Satyaki PRV, Moeglein M, et al. 2020.. Water lily. . PNAS 117::864956
    [Crossref] [Google Scholar]
  113. 113.
    Quarrie SA, Jones HG. 1977.. Effects of abscisic acid and water stress on development and morphology of wheat. . J. Exp. Bot. 28::192203
    [Crossref] [Google Scholar]
  114. 114.
    Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M. 2016.. Molecular and genetic control of plant thermomorphogenesis. . Nat. Plants 2::15190
    [Crossref] [Google Scholar]
  115. 115.
    Rao SK, Magnin NlC, Reiskind JB, Bowes G. 2002.. Photosynthetic and other phosphoenolpyruvate carboxylase isoforms in the single-cell, facultative C4 system of Hydrilla verticillata. . Plant Physiol. 130::87686
    [Crossref] [Google Scholar]
  116. 116.
    Rascio H, Cuccato F, Vecchia FD, Rocca HL, Larcher W. 1999.. Structural and functional features of the leaves of Ranunculus trichophyllus Chaix., a freshwater submerged macrophophyte. . Plant Cell Environ. 22::20512
    [Crossref] [Google Scholar]
  117. 117.
    Raven JA. 1970.. Exogenous inorganic carbon sources in plant photosynthesis. . Biol. Rev. 45::167220
    [Crossref] [Google Scholar]
  118. 118.
    Raven JA. 2002.. Selection pressures on stomatal evolution. . New Phytol. 153::37186
    [Crossref] [Google Scholar]
  119. 119.
    Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM. 2004.. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. . Development 131::422537
    [Crossref] [Google Scholar]
  120. 120.
    Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, et al. 2003.. Regulation of phyllotaxis by polar auxin transport. . Nature 426::25560
    [Crossref] [Google Scholar]
  121. 121.
    Ronzhina DA, P'Yankov VI. 2001.. Structure of the photosynthetic apparatus in leaves of freshwater hydrophytes: 1. General characteristics of the leaf mesophyll and a comparison with terrestrial plants. . Russ. J. Plant Physiol. 48::56775
    [Crossref] [Google Scholar]
  122. 122.
    Sakamoto T, Ikematsu S, Namie K, Hou H, Li G, Kimura S. 2022.. Leaf cell morphology alternation in response to environmental signals in Rorippa aquatica. . Int. J. Mol. Sci. 23::10401
    [Crossref] [Google Scholar]
  123. 123.
    Schenck H. 1886.. Vergleichende anatomie der submersen gewächse. . Biblio. Bot. 1::167
    [Google Scholar]
  124. 124.
    Sculthorpe CD. 1967.. The Biology of Aquatic Vascular Plants. London:: Edward Arnold
    [Google Scholar]
  125. 125.
    Serna L, Fenoll C. 1996.. Ethylene induces stomata differentiation in Arabidopsis. . Int. J. Dev. Biol. 40:(Suppl. 1):12324
    [Google Scholar]
  126. 126.
    Sperry JS. 2003.. Evolution of water transport and xylem structure. . Int. J. Plant Sci. 164::11527
    [Crossref] [Google Scholar]
  127. 127.
    Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, et al. 2010.. Stomagen positively regulates stomatal density in Arabidopsis. . Nature 463::24144
    [Crossref] [Google Scholar]
  128. 128.
    Tanaka Y, Nose T, Jikumaru Y, Kamiya Y. 2013.. ABA inhibits entry into stomatal-lineage development in Arabidopsis leaves. . Plant J. 74::44857
    [Crossref] [Google Scholar]
  129. 129.
    Toriba T, Tokunaga H, Shiga T, Nie F, Naramoto S, et al. 2019.. BLADE-ON-PETIOLE genes temporally and developmentally regulate the sheath to blade ratio of rice leaves. . Nat. Commun. 10::619
    [Crossref] [Google Scholar]
  130. 130.
    Torii KU. 2012.. Mix-and-match: ligand–receptor pairs in stomatal development and beyond. . Trends Plant Sci. 17::71119
    [Crossref] [Google Scholar]
  131. 131.
    Tsukaya H. 2002.. Leaf development. . Arabidopsis Book 1::e0072
    [Crossref] [Google Scholar]
  132. 132.
    Tsukaya H. 2018.. A consideration of leaf shape evolution in the context of the primary function of the leaf as a photosynthetic organ. . In The Leaf: A Platform for Performing Photosynthesis, ed. WW Adams III, I Terashima , pp. 126. Cham, Switz:.: Springer Int.
    [Google Scholar]
  133. 133.
    Tsukaya H. 2018.. Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation. . Semin. Cell Dev. Biol. 79::4857
    [Crossref] [Google Scholar]
  134. 134.
    Tsukaya H. 2021.. The leaf meristem enigma: the relationship between the plate meristem and the marginal meristem. . Plant Cell 33::3194206
    [Crossref] [Google Scholar]
  135. 135.
    Tsukaya H, Shoda K, Kim G-T, Uchimiya H. 2000.. Heteroblasty in Arabidopsis thaliana (L.) Heynh. . Planta 210::53642
    [Crossref] [Google Scholar]
  136. 136.
    Ueno O. 2001.. Environmental regulation of C3 and C4 differentiation in the amphibious sedge Eleocharis vivipara. . Plant Physiol. 127::152432
    [Crossref] [Google Scholar]
  137. 137.
    Ueno O, Samejima M, Muto S, Miyachi S. 1988.. Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. . PNAS 85::673337 137. Shows that Eleocharis vivipara undergoes C3 photosynthesis in water and C4 photosynthesis on land, with Kranz structure in aerial leaves.
    [Crossref] [Google Scholar]
  138. 138.
    van der Valk AG. 2006.. The Biology of Freshwater Wetlands. New York:: Oxford Univ. Press
    [Google Scholar]
  139. 139.
    van Veen H, Mustroph A, Barding GA, Vergeer-van Eijk M, Welschen-Evertman RAM, et al. 2013.. Two Rumex species from contrasting hydrological niches regulate flooding tolerance through distinct mechanisms. . Plant Cell 25::4691747
    [Crossref] [Google Scholar]
  140. 140.
    van Veen H, Sasidharan R. 2021.. Shape shifting by amphibious plants in dynamic hydrological niches. . New Phytol. 229::7984
    [Crossref] [Google Scholar]
  141. 141.
    Wang H, Kong F, Zhou C. 2021.. From genes to networks: the genetic control of leaf development. . J. Integr. Plant Biol. 63::118196
    [Crossref] [Google Scholar]
  142. 142.
    Wanke D. 2011.. The ABA-mediated switch between submersed and emersed life-styles in aquatic macrophytes. . J. Plant Res. 124::46775
    [Crossref] [Google Scholar]
  143. 143.
    Wellman CH. 2010.. The invasion of the land by plants: when and where?. New Phytol. 188::30911
    [Crossref] [Google Scholar]
  144. 144.
    Wells CL, Pigliucci M. 2000.. Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants. . Perspect. Plant Ecol. Evol. Syst. 3::118
    [Crossref] [Google Scholar]
  145. 145.
    West-Eberhard MJ. 2003.. Developmental Plasticity and Evolution. New York:: Oxford Univ. Press
    [Google Scholar]
  146. 146.
    Wickell D, Kuo L-Y, Yang H-P, Ashok AD, Irisarri I, et al. 2021.. Underwater CAM photosynthesis elucidated by Isoetes genome. . Nat. Commun. 12::6348
    [Crossref] [Google Scholar]
  147. 147.
    Wiegleb G. 1988.. Notes on Japanese Ranunculus subgenus Batrachium. . Acta Phytotax. Geobot. 39::11732
    [Google Scholar]
  148. 148.
    Yin L, Li W, Madsen TV, Maberly SC, Bowes G. 2017.. Photosynthetic inorganic carbon acquisition in 30 freshwater macrophytes. . Aquat. Bot. 140::4854
    [Crossref] [Google Scholar]
  149. 149.
    Young JP, Dengler NG, Horton RF. 1987.. Heterophylly in Ranunculus flabellaris: the effect of abscisic acid on leaf anatomy. . Ann. Bot. 60::11725
    [Crossref] [Google Scholar]
  150. 150.
    Zhang L, Chen F, Zhang X, Li Z, Zhao Y, et al. 2020.. The water lily genome and the early evolution of flowering plants. . Nature 577::7984
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-arplant-062923-024919
Loading
/content/journals/10.1146/annurev-arplant-062923-024919
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error