C-4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation

Carregando...
Imagem de Miniatura
Citações na Scopus
25
Tipo de produção
article
Data de publicação
2020
Título da Revista
ISSN da Revista
Título do Volume
Editora
WILEY
Autores
FERRARI, Renata C.
BITTENCOURT, Priscila P.
RODRIGUES, Maria A.
MORENO-VILLENA, Jose J.
ALVES, Frederico R. R.
BOXALL, Susanna F.
DEVER, Louisa V.
DEMARCO, Diego
ANDRADE, Sonia C. S.
Citação
NEW PHYTOLOGIST, v.225, n.4, p.1699-1714, 2020
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Although biochemically related, C-4 and crassulacean acid metabolism (CAM) systems are expected to be incompatible. However, Portulaca species, including P. oleracea, operate C-4 and CAM within a single leaf, and the mechanisms behind this unique photosynthetic arrangement remain largely unknown. Here, we employed RNA-seq to identify candidate genes involved exclusively or shared by C-4 or CAM, and provided an in-depth characterization of their transcript abundance patterns during the drought-induced photosynthetic transitions in P. oleracea. Data revealed fewer candidate CAM-specific genes than those recruited to function in C-4. The putative CAM-specific genes were predominantly involved in night-time primary carboxylation reactions and malate movement across the tonoplast. Analysis of gene transcript-abundance regulation and photosynthetic physiology indicated that C-4 and CAM coexist within a single P. oleracea leaf under mild drought conditions. Developmental and environmental cues were shown to regulate CAM expression in stems, whereas the shift from C-4 to C-4-CAM hybrid photosynthesis in leaves was strictly under environmental control. Moreover, efficient starch turnover was identified as part of the metabolic adjustments required for CAM operation in both organs. These findings provide insights into C-4/CAM connectivity and compatibility, contributing to a deeper understanding of alternative ways to engineer CAM into C-4 crop species.
Palavras-chave
C-4, crassulacean acid metabolism, drought stress, facultative CAM, Portulaca oleracea, RNA-seq, transcriptome
Referências
  1. ADAMS WW, 1988, PLANT PHYSIOL, V86, P117, DOI 10.1104/pp.86.1.117
  2. Black CC, 1996, ECOL STU AN, V114, P31
  3. Bohnert HJ, 2000, J PLANT GROWTH REGUL, V19, P334, DOI 10.1007/s003440000033
  4. Borland AM, 2016, CURR OPIN PLANT BIOL, V31, P118, DOI 10.1016/j.pbi.2016.04.001
  5. Borland AM, 2009, J EXP BOT, V60, P2879, DOI 10.1093/jxb/erp118
  6. Boxall SF, 2019, SILENCING PHOSPHOENO
  7. Boxall SF, 2017, PLANT CELL, V29, P2519, DOI 10.1105/tpc.17.00301
  8. Brautigam A, 2017, PLANT PHYSIOL, V174, P473, DOI 10.1104/pp.17.00195
  9. Brilhaus D, 2016, PLANT PHYSIOL, V170, P102, DOI 10.1104/pp.15.01076
  10. CARTER PJ, 1991, EMBO J, V10, P2063, DOI 10.1002/j.1460-2075.1991.tb07737.x
  11. Chastain CJ, 2003, PLANT PHYSIOL BIOCH, V41, P523, DOI 10.1016/S0981-9428(03)00065-2
  12. Chastain CJ, 2002, PLANT PHYSIOL, V128, P1368, DOI 10.1104/pp.010806
  13. Chen ZH, 2012, PLANT PHYSIOL, V159, P1235, DOI 10.1104/pp.112.197350
  14. Christin PA, 2015, MOL BIOL EVOL, V32, P846, DOI 10.1093/molbev/msu410
  15. Christin PA, 2014, J EXP BOT, V65, P3609, DOI 10.1093/jxb/eru087
  16. Covshoff S, 2012, CURR OPIN BIOTECH, V23, P209, DOI 10.1016/j.copbio.2011.12.011
  17. Cruz AB, 2018, FRONT PLANT SCI, V9, DOI 10.3389/fpls.2018.01370
  18. Cushman JC, 2008, J EXP BOT, V59, P1875, DOI 10.1093/jxb/ern008
  19. De Angeli A, 2013, NATURE COMMUNICATION, V4, P1
  20. Dever LV, 2015, PLANT PHYSIOL, V167, P44, DOI 10.1104/pp.114.251827
  21. Edwards EJ, 2019, NEW PHYTOL, V223, P1742, DOI 10.1111/nph.15851
  22. Edwards EJ, 2012, INT J PLANT SCI, V173, P724, DOI 10.1086/666098
  23. Ferrari RC, 2019, PLANT SIGNALING MOLECULES: ROLE AND REGULATION UNDER STRESSFUL ENVIRONMENTS, P517, DOI 10.1016/B978-0-12-816451-8.00032-0
  24. Freschi L, 2010, J PLANT PHYSIOL, V167, P1577, DOI 10.1016/j.jplph.2010.06.002
  25. Fukao Y, 2002, PLANT CELL PHYSIOL, V43, P689, DOI 10.1093/pcp/pcf101
  26. Furbank RT, 2011, J EXP BOT, V62, P3103, DOI 10.1093/jxb/err080
  27. Furumoto T, 2011, NATURE, V476, P472, DOI 10.1038/nature10250
  28. Gonnella M., 2010, EUR J PLANT SCI BIOT, V4, P131
  29. GRIFFITHS H, 1989, ECOL STU AN, V76, P42
  30. Guralnick LJ, 2001, INT J PLANT SCI, V162, P257, DOI 10.1086/319569
  31. Hafke JB, 2003, PLANT J, V35, P116, DOI 10.1046/j.1365-313X.2003.01781.x
  32. Haider MS, 2012, J EXP BOT, V63, P1985, DOI 10.1093/jxb/err412
  33. Hartwell J, 1999, PLANT J, V20, P333, DOI 10.1046/j.1365-313X.1999.t01-1-00609.x
  34. Hartwell J, 1996, PLANT J, V10, P1071, DOI 10.1046/j.1365-313X.1996.10061071.x
  35. Hartwell J, 2005, ANNU PLANT REV, V21, P211
  36. Hartwell J, 2016, CURR OPIN PLANT BIOL, V31, P100, DOI 10.1016/j.pbi.2016.03.019
  37. HATCH MD, 1987, BIOCHIM BIOPHYS ACTA, V895, P81, DOI 10.1016/S0304-4173(87)80009-5
  38. Herrera A, 2009, ANN BOT-LONDON, V103, P645, DOI 10.1093/aob/mcn145
  39. Hibberd JM, 2010, ANNU REV PLANT BIOL, V61, P181, DOI 10.1146/annurev-arplant-042809-112238
  40. Holtum JAM, 2017, J PLANT PHYSIOL, V214, P91, DOI 10.1016/j.jplph.2017.01.010
  41. Kajala K, 2011, J EXP BOT, V62, P3001, DOI 10.1093/jxb/err022
  42. KANAI R, 1999, C4 PLANT BIOL, P49
  43. Keeley JE, 2003, INT J PLANT SCI, V164, pS55, DOI 10.1086/374192
  44. KOCH K, 1980, PLANT PHYSIOL, V65, P193, DOI 10.1104/pp.65.2.193
  45. KOCH KE, 1982, PLANT PHYSIOL, V69, P757, DOI 10.1104/pp.69.4.757
  46. Kovermann P, 2007, PLANT J, V52, P1169, DOI 10.1111/j.1365-313X.2007.03367.x
  47. KU SB, 1981, PLANT PHYSIOL, V68, P1073, DOI 10.1104/pp.68.5.1073
  48. LAETSCH WM, 1968, AM J BOT, V55, P875, DOI 10.2307/2440550
  49. Lara MV, 2004, PLANT CELL PHYSIOL, V45, P618, DOI 10.1093/pcp/pch073
  50. Lara MV, 2003, PHOTOSYNTH RES, V77, P241, DOI 10.1023/A:1025834120499
  51. D'Andrea RM, 2014, PHYSIOL PLANTARUM, V152, P414, DOI 10.1111/ppl.12194
  52. MATSUOKA M, 1995, PLANT CELL PHYSIOL, V36, P937, DOI 10.1093/oxfordjournals.pcp.a078864
  53. Mazen AMA, 1996, PHYSIOL PLANTARUM, V98, P111, DOI 10.1111/j.1399-3054.1996.tb00681.x
  54. Mazen AMA, 2000, PHOTOSYNTHETICA, V38, P385, DOI 10.1023/A:1010969419962
  55. Meyer S, 2010, PLANT J, V63, P1054, DOI 10.1111/j.1365-313X.2010.04302.x
  56. MIYANISHI K, 1980, CAN J PLANT SCI, V60, P953, DOI 10.4141/cjps80-139
  57. Monne M, 2018, J BIOL CHEM, V293, P4213, DOI 10.1074/jbc.RA117.000771
  58. Moreno-Villena JJ, 2018, MOL BIOL EVOL, V35, P94, DOI 10.1093/molbev/msx269
  59. Nelson EA, 2005, FUNCT PLANT BIOL, V32, P409, DOI 10.1071/FP04195
  60. Neuhaus HE, 1996, BIOCHEM J, V318, P945, DOI 10.1042/bj3180945
  61. Nimmo HG, 2001, NEW PHYTOL, V151, P91, DOI 10.1046/j.1469-8137.2001.00155.x
  62. OSMOND CB, 1978, ANNU REV PLANT PHYS, V29, P379, DOI 10.1146/annurev.pp.29.060178.002115
  63. Palmieri L, 2008, BIOCHEM J, V410, P621, DOI 10.1042/BJ20070867
  64. Alves FRR, 2016, ACTA PHYSIOL PLANT, V38, DOI 10.1007/s11738-016-2169-8
  65. Sage RF, 2002, FUNCT PLANT BIOL, V29, P775, DOI 10.1071/PP01217
  66. Sage Rowan F, 2017, J Exp Bot, V68, P4039, DOI 10.1093/jxb/erx005
  67. Schluter U, 2016, CURR OPIN PLANT BIOL, V31, P83, DOI 10.1016/j.pbi.2016.03.007
  68. SCHULTZ CJ, 1995, PLANT J, V7, P61, DOI 10.1046/j.1365-313X.1995.07010061.x
  69. Silvera K, 2010, FUNCT PLANT BIOL, V37, P995, DOI 10.1071/FP10084
  70. Smith JAC, 1996, ECOL STU AN, V114, P53
  71. Taylor SH, 2014, GLOBAL CHANGE BIOL, V20, P1992, DOI 10.1111/gcb.12498
  72. THOMPSON AG, 1987, BIOCHEM BIOPH RES CO, V143, P164, DOI 10.1016/0006-291X(87)90645-0
  73. Amaral Lourdes Isabel Velho do, 2007, Hoehnea, V34, P425, DOI 10.1590/S2236-89062007000400001
  74. Voznesenskaya EV, 2010, J EXP BOT, V61, P3647, DOI 10.1093/jxb/erq178
  75. Voznesenskaya EV, 2002, PLANT J, V31, P649, DOI 10.1046/j.1365-313X.2002.01385.x
  76. Voznesenskaya EV, 2001, NATURE, V414, P543, DOI 10.1038/35107073
  77. Vozza A, 2014, P NATL ACAD SCI USA, V111, P960, DOI 10.1073/pnas.1317400111
  78. Wai CM, 2019, PLOS GENET, V15, DOI 10.1371/journal.pgen.1008209
  79. Weise SE, 2011, J EXP BOT, V62, P3109, DOI 10.1093/jxb/err035
  80. Wheeler MCG, 2005, PLANT PHYSIOL, V139, P39, DOI 10.1104/pp.105.065953
  81. Wilkie SE, 1998, PROTEIN EXPRES PURIF, V12, P381, DOI 10.1006/prep.1997.0845
  82. Winter K, 1996, ECOL STUD-ANAL SYNTH, V114, P1
  83. Winter K, 2017, AUSTR J BOT, V65, P3425
  84. Winter K, 2019, J EXP BOT, V70, P6571, DOI 10.1093/jxb/erz085
  85. Winter K, 2019, J EXP BOT, V70, P6495, DOI 10.1093/jxb/erz002
  86. Winter K, 2014, J EXP BOT, V65, P3425, DOI 10.1093/jxb/eru063
  87. Yang XH, 2015, NEW PHYTOL, V207, P491, DOI 10.1111/nph.13393
  88. Zhang JB, 2013, PLANT PHYSIOL, V163, P830, DOI 10.1104/pp.113.219832
  89. ZIMMERMAN CA, 1976, ECOLOGY, V57, P964, DOI 10.2307/1941061