Tolerance to Cyclic Desiccation in Lichen Microalgae is Related to Habitat Preference and Involves Specific Priming of the Antioxidant System

Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9)...

Full description

Saved in:
Bibliographic Details
Published inPlant and cell physiology Vol. 60; no. 8; pp. 1880 - 1891
Main Authors Hell, Aline F, Gasulla, Francisco, Gonz lez-Hourcade, Mar a, del Campo, Eva M, Centeno, Danilo C, Casano, Leonardo M
Format Journal Article
LanguageEnglish
Published Japan 01.08.2019
Subjects
Online AccessGet full text
ISSN0032-0781
1471-9053
1471-9053
DOI10.1093/pcp/pcz103

Cover

Loading…
Abstract Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9) and Coccomyxa simplex (Csol), were analyzed. TR9 was isolated from Ramalina farinacea, a Mediterranean fruticose epiphytic lichen adapted to xeric habitats, while Csol is the phycobiont of Solorina saccata, a foliaceous lichen that grows on humid rock crevices. The tolerance to desiccation of both species was tested by subjecting them to different drying conditions and to four consecutive daily cycles of D/R. Our results show that a relative humidity close to that of their habitats was crucial to maintain the photosynthetic rates. Concerning antioxidant enzymes, in general, manganese superoxide dismutases (MnSODs) were induced after desiccation and decreased after rehydration. In TR9, catalase (CAT)-A increased, and its activity was maintained after four cycles of D/R. Ascorbate peroxidase activity was detected only in Csol, while glutathione reductase increased only in TR9. Transcript levels of antioxidant enzymes indicate that most isoforms of MnSOD and FeSOD were induced by desiccation and repressed after rehydration. CAT2 gene expression was also upregulated and maintained at higher levels even after four cycles of D/R in accordance with enzymatic activities. To our knowledge, this is the first study to include the complete set of the main antioxidant enzymes in desiccation-tolerant microalgae. The results highlight the species-specific induction of the antioxidant system during cyclic D/R, suggesting a priming of oxidative defence metabolism.
AbstractList Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9) and Coccomyxa simplex (Csol), were analyzed. TR9 was isolated from Ramalina farinacea, a Mediterranean fruticose epiphytic lichen adapted to xeric habitats, while Csol is the phycobiont of Solorina saccata, a foliaceous lichen that grows on humid rock crevices. The tolerance to desiccation of both species was tested by subjecting them to different drying conditions and to four consecutive daily cycles of D/R. Our results show that a relative humidity close to that of their habitats was crucial to maintain the photosynthetic rates. Concerning antioxidant enzymes, in general, manganese superoxide dismutases (MnSODs) were induced after desiccation and decreased after rehydration. In TR9, catalase (CAT)-A increased, and its activity was maintained after four cycles of D/R. Ascorbate peroxidase activity was detected only in Csol, while glutathione reductase increased only in TR9. Transcript levels of antioxidant enzymes indicate that most isoforms of MnSOD and FeSOD were induced by desiccation and repressed after rehydration. CAT2 gene expression was also upregulated and maintained at higher levels even after four cycles of D/R in accordance with enzymatic activities. To our knowledge, this is the first study to include the complete set of the main antioxidant enzymes in desiccation-tolerant microalgae. The results highlight the species-specific induction of the antioxidant system during cyclic D/R, suggesting a priming of oxidative defence metabolism.Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9) and Coccomyxa simplex (Csol), were analyzed. TR9 was isolated from Ramalina farinacea, a Mediterranean fruticose epiphytic lichen adapted to xeric habitats, while Csol is the phycobiont of Solorina saccata, a foliaceous lichen that grows on humid rock crevices. The tolerance to desiccation of both species was tested by subjecting them to different drying conditions and to four consecutive daily cycles of D/R. Our results show that a relative humidity close to that of their habitats was crucial to maintain the photosynthetic rates. Concerning antioxidant enzymes, in general, manganese superoxide dismutases (MnSODs) were induced after desiccation and decreased after rehydration. In TR9, catalase (CAT)-A increased, and its activity was maintained after four cycles of D/R. Ascorbate peroxidase activity was detected only in Csol, while glutathione reductase increased only in TR9. Transcript levels of antioxidant enzymes indicate that most isoforms of MnSOD and FeSOD were induced by desiccation and repressed after rehydration. CAT2 gene expression was also upregulated and maintained at higher levels even after four cycles of D/R in accordance with enzymatic activities. To our knowledge, this is the first study to include the complete set of the main antioxidant enzymes in desiccation-tolerant microalgae. The results highlight the species-specific induction of the antioxidant system during cyclic D/R, suggesting a priming of oxidative defence metabolism.
Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress are still being unraveled. Therefore, the physiological performance and antioxidant mechanisms of two lichen microalgae, Trebouxia sp. (TR9) and Coccomyxa simplex (Csol), were analyzed. TR9 was isolated from Ramalina farinacea, a Mediterranean fruticose epiphytic lichen adapted to xeric habitats, while Csol is the phycobiont of Solorina saccata, a foliaceous lichen that grows on humid rock crevices. The tolerance to desiccation of both species was tested by subjecting them to different drying conditions and to four consecutive daily cycles of D/R. Our results show that a relative humidity close to that of their habitats was crucial to maintain the photosynthetic rates. Concerning antioxidant enzymes, in general, manganese superoxide dismutases (MnSODs) were induced after desiccation and decreased after rehydration. In TR9, catalase (CAT)-A increased, and its activity was maintained after four cycles of D/R. Ascorbate peroxidase activity was detected only in Csol, while glutathione reductase increased only in TR9. Transcript levels of antioxidant enzymes indicate that most isoforms of MnSOD and FeSOD were induced by desiccation and repressed after rehydration. CAT2 gene expression was also upregulated and maintained at higher levels even after four cycles of D/R in accordance with enzymatic activities. To our knowledge, this is the first study to include the complete set of the main antioxidant enzymes in desiccation-tolerant microalgae. The results highlight the species-specific induction of the antioxidant system during cyclic D/R, suggesting a priming of oxidative defence metabolism.
Author Gasulla, Francisco
Hell, Aline F
Centeno, Danilo C
Gonz lez-Hourcade, Mar a
Casano, Leonardo M
del Campo, Eva M
Author_xml – sequence: 1
  givenname: Aline F
  surname: Hell
  fullname: Hell, Aline F
– sequence: 2
  givenname: Francisco
  surname: Gasulla
  fullname: Gasulla, Francisco
– sequence: 3
  givenname: Mar a
  surname: Gonz lez-Hourcade
  fullname: Gonz lez-Hourcade, Mar a
– sequence: 4
  givenname: Eva M
  surname: del Campo
  fullname: del Campo, Eva M
– sequence: 5
  givenname: Danilo C
  surname: Centeno
  fullname: Centeno, Danilo C
– sequence: 6
  givenname: Leonardo M
  orcidid: 0000-0002-2304-7317
  surname: Casano
  fullname: Casano, Leonardo M
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31127294$$D View this record in MEDLINE/PubMed
BookMark eNptkc1uFDEQhC0URDaBCw-AfERIA_6ZxDPHaAMk0iIiEs5WT7udGM3aw9gbsXmHvDNebXJBHKz2oapa_dURO4gpEmNvpfgoRa8_TTjV9yCFfsEWsjWy6cWJPmALIbRqhOnkITvK-ZcQ9a_FK3aopVRG9e2CPd6kkWaISLwkvtziGJCfUw6IUEKKPES-CnhHkX8LOCcYb4F4yPwHjVDI7VwXMIQChV_N5GmmXRZExy_jfRrvKfPriTD4mns1h3WItzx5Xu6In8W64U9wEAu_3uZC69fspYcx05unecx-fvl8s7xoVt-_Xi7PVg2qzpSmR-Wd1ENrBiE8UYdu0OBkrxGc81L2CrEzDqCFFsn7QRlxOnTDqdQdotLH7P0-d5rT7w3lYtchI40jREqbbJXSSnTmxJgqffck3QxrcnaqN8C8tc8Iq0DsBZVOzhWBxR2Nyq7MEEYrhd21ZGtLdt9StXz4x_Kc-h_xX0pXl3Y
CitedBy_id crossref_primary_10_1016_j_envexpbot_2021_104397
crossref_primary_10_1007_s00248_021_01685_z
crossref_primary_10_1142_S0218339021400052
crossref_primary_10_1134_S1021443722602798
crossref_primary_10_1111_1462_2920_15043
crossref_primary_10_1111_nph_18048
crossref_primary_10_3390_plants12234011
crossref_primary_10_1007_s00248_023_02213_x
crossref_primary_10_1111_jpy_12928
crossref_primary_10_3390_plants10040807
crossref_primary_10_1111_ppl_13402
crossref_primary_10_21285_2227_2925_2023_13_4_532_544
crossref_primary_10_3390_life12060817
crossref_primary_10_1007_s00248_020_01604_8
crossref_primary_10_1007_s13199_024_00982_8
crossref_primary_10_1007_s13199_024_00985_5
crossref_primary_10_1016_j_bbrc_2023_02_079
crossref_primary_10_3390_microorganisms10122444
crossref_primary_10_1093_aob_mcz181
Cites_doi 10.1007/s11103-016-0468-5
10.1128/AEM.71.4.2121-2129.2005
10.1093/aob/mcq206
10.1046/j.0016-8025.2003.01052.x
10.1186/gb-2002-3-7-research0034
10.1111/1462-2920.13249
10.1007/s00425-009-1019-y
10.1111/j.1365-3040.2007.01704.x
10.1016/S1360-1385(01)02086-6
10.1016/j.plaphy.2010.08.016
10.1093/jxb/erw382
10.1017/S0024282986000075
10.1016/0003-2697(71)90375-7
10.1093/icb/45.5.734
10.1007/BF00422045
10.1016/j.bbabio.2009.11.007
10.1111/j.1365-3040.2011.02400.x
10.1016/j.jplph.2018.05.002
10.1073/pnas.0407716102
10.1046/j.1469-8137.2003.00852.x
10.1639/0007-2745-111.4.576
10.1093/pcp/pcw111
10.1111/j.1365-313X.2007.03263.x
10.1016/j.jplph.2012.07.005
10.1006/lich.1996.0034
10.1155/2017/7243973
10.1007/s13199-015-0330-6
10.1023/B:PHOT.0000027522.35486.f6
10.1007/s00018-012-1155-6
10.1016/j.bbabio.2012.02.036
10.1111/j.1399-3054.2010.01417.x
10.1186/1471-2180-10-297
10.3389/fpls.2013.00482
10.3389/fpls.2016.01279
10.1371/journal.pone.0110630
10.1016/j.plaphy.2018.06.004
10.1111/j.1462-2920.2010.02386.x
10.1007/s00425-010-1129-6
10.2174/1389203715666140327105143
10.1093/jexbot/53.372.1305
10.1016/j.plaphy.2017.02.021
10.1128/AEM.71.11.6508-6514.2005
10.14348/molcells.2016.2324
10.1007/978-1-4020-3218-9_3
10.1023/A:1026534305831
10.1046/j.1469-8137.2002.00376.x
10.1002/j.1460-2075.1985.tb03949.x
10.1055/s-2007-965580
10.1007/s10811-010-9631-6
10.1111/tpj.12008
10.1023/A:1005863015130
10.1104/pp.59.5.1011
10.1046/j.1365-313X.2002.01329.x
10.1016/0003-2697(76)90527-3
10.1007/s00248-014-0524-0
10.1016/j.pbi.2011.03.018
10.1111/nph.15488
ContentType Journal Article
Copyright � The Author(s) 2019. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.
Copyright_xml – notice: � The Author(s) 2019. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1093/pcp/pcz103
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
CrossRef
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
Botany
EISSN 1471-9053
EndPage 1891
ExternalDocumentID 31127294
10_1093_pcp_pcz103
Genre Journal Article
GroupedDBID ---
-E4
-~X
.2P
.I3
0R~
123
1TH
29O
2WC
4.4
482
48X
5VS
5WD
6P2
70D
A8Z
AAHBH
AAIMJ
AAJKP
AAKDD
AAMDB
AAMVS
AAOGV
AAPQZ
AAPXW
AARHZ
AAUAY
AAUQX
AAVAP
AAVLN
AAYXX
ABDBF
ABDFA
ABEJV
ABEUO
ABGNP
ABIXL
ABJNI
ABMNT
ABNKS
ABPQP
ABPTD
ABQLI
ABVGC
ABWST
ABXVV
ABXZS
ABZBJ
ACGFS
ACIWK
ACNCT
ACPRK
ACUFI
ACUHS
ACUTJ
ADBBV
ADEYI
ADEZT
ADFTL
ADGKP
ADGZP
ADHKW
ADHZD
ADIPN
ADNBA
ADOCK
ADQBN
ADRTK
ADVEK
ADYVW
ADZTZ
ADZXQ
AEGPL
AEJOX
AEKSI
AELWJ
AEMDU
AENEX
AENZO
AEPUE
AETBJ
AEWNT
AFFZL
AFGWE
AFIYH
AFOFC
AFRAH
AGINJ
AGKEF
AGORE
AGQXC
AGSYK
AHGBF
AHMBA
AHXPO
AIJHB
AJBYB
AJEEA
AJNCP
AKHUL
AKWXX
ALMA_UNASSIGNED_HOLDINGS
ALUQC
ALXQX
APIBT
APWMN
ARIXL
ATGXG
AXUDD
AYOIW
BAWUL
BAYMD
BCRHZ
BEYMZ
BHONS
BQDIO
BSWAC
CDBKE
CITATION
CS3
CZ4
DAKXR
DIK
DILTD
DU5
D~K
EBD
EBS
ECGQY
EDH
EE~
EJD
EMOBN
ESX
F5P
F9B
FHSFR
FLUFQ
FOEOM
FQBLK
GAUVT
GJXCC
H13
H5~
HAR
HW0
HZ~
IOX
J21
JXSIZ
KAQDR
KBUDW
KOP
KQ8
KSI
KSN
M-Z
N9A
NGC
NLBLG
NOMLY
NU-
O9-
OAWHX
OBOKY
ODMLO
OJQWA
OJZSN
OK1
OWPYF
P2P
PAFKI
PEELM
PQQKQ
Q1.
Q5Y
R44
RD5
ROL
ROX
ROZ
RUSNO
RW1
RXO
SV3
TLC
TN5
TUS
TWZ
W8F
X7H
Y6R
YAYTL
YKOAZ
YNT
YSK
YXANX
ZKX
~91
~KM
CGR
CUY
CVF
ECM
EIF
M49
NPM
7X8
ID FETCH-LOGICAL-c287t-9c2fd13b47b00fee8cdb3ad193caddf1192cc87daa4a4ceffb2706b8b6138cc23
ISSN 0032-0781
1471-9053
IngestDate Fri Jul 11 05:57:38 EDT 2025
Thu Apr 03 07:09:39 EDT 2025
Tue Jul 01 02:34:00 EDT 2025
Thu Apr 24 23:01:50 EDT 2025
IsPeerReviewed true
IsScholarly true
Issue 8
Keywords Priming
Trebouxia
Desiccation tolerance
Coccomyxa
Lichen microalga
Antioxidant
Language English
License https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model
� The Author(s) 2019. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c287t-9c2fd13b47b00fee8cdb3ad193caddf1192cc87daa4a4ceffb2706b8b6138cc23
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-2304-7317
PMID 31127294
PQID 2232087577
PQPubID 23479
PageCount 12
ParticipantIDs proquest_miscellaneous_2232087577
pubmed_primary_31127294
crossref_citationtrail_10_1093_pcp_pcz103
crossref_primary_10_1093_pcp_pcz103
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-08-01
2019-Aug-01
20190801
PublicationDateYYYYMMDD 2019-08-01
PublicationDate_xml – month: 08
  year: 2019
  text: 2019-08-01
  day: 01
PublicationDecade 2010
PublicationPlace Japan
PublicationPlace_xml – name: Japan
PublicationTitle Plant and cell physiology
PublicationTitleAlternate Plant Cell Physiol
PublicationYear 2019
References Gray (2023052516423494300_pcz103-B30) 2007; 30
Woodbury (2023052516423494300_pcz103-B61) 1971; 44
Carniel (2023052516423494300_pcz103-B9) 2016; 91
Yobi (2023052516423494300_pcz103-B62) 2012; 72
del Hoyo (2023052516423494300_pcz103-B15) 2011; 107
Roach (2023052516423494300_pcz103-B51) 2014; 15
Holzinger (2023052516423494300_pcz103-B32) 2014; 9
Komura (2023052516423494300_pcz103-B35) 2010; 1797
Mubarakshina Borisova (2023052516423494300_pcz103-B46) 2012; 1817
Mayaba (2023052516423494300_pcz103-B45) 2001; 31
Oliver (2023052516423494300_pcz103-B48) 1998; 24
Dinakar (2023052516423494300_pcz103-B17) 2013; 4
Vandesompele (2023052516423494300_pcz103-B57) 2002; 3
Farrant (2023052516423494300_pcz103-B20) 2003; 26
Dietz (2023052516423494300_pcz103-B16) 2016; 39
lvarez (2023052516423494300_pcz103-B3) 2012; 169
Baker (2023052516423494300_pcz103-B5) 2004
Maruta (2023052516423494300_pcz103-B44) 2016; 57
Filippou (2023052516423494300_pcz103-B23) 2013
Queval (2023052516423494300_pcz103-B49) 2007; 52
Kranner (2023052516423494300_pcz103-B38) 2008; 111
Farrant (2023052516423494300_pcz103-B18) 2000; 151
Gechev (2023052516423494300_pcz103-B27) 2013; 70
Shigeoka (2023052516423494300_pcz103-B53) 2002; 53
Gasulla (2023052516423494300_pcz103-B25) 2016; 57
Gill (2023052516423494300_pcz103-B29) 2010; 48
Bradford (2023052516423494300_pcz103-B8) 1976; 72
Zhou (2023052516423494300_pcz103-B63) 2017; 2017
Krog (2023052516423494300_pcz103-B43) 1986; 18
Feng (2023052516423494300_pcz103-B21) 2016; 7
Heber (2023052516423494300_pcz103-B31) 2011; 142
Noctor (2023052516423494300_pcz103-B47) 2012; 35
Farrant (2023052516423494300_pcz103-B19) 2011; 14
Smirnoff (2023052516423494300_pcz103-B55) 2019; 221
Casano (2023052516423494300_pcz103-B10) 2011; 13
Kranner (2023052516423494300_pcz103-B42) 2003; 160
Bold (2023052516423494300_pcz103-B7) 1962; 42
Alscher (2023052516423494300_pcz103-B1) 2002; 53
da Costa (2023052516423494300_pcz103-B14) 2015; 66
Centeno (2023052516423494300_pcz103-B12) 2016; 18
Gasulla (2023052516423494300_pcz103-B26) 2009; 231
Rausch (2023052516423494300_pcz103-B50) 2007; 9
Kouřil (2023052516423494300_pcz103-B36) 2003; 41
Weissman (2023052516423494300_pcz103-B59) 2005; 71
Wang (2023052516423494300_pcz103-B58) 2011; 23
Kranner (2023052516423494300_pcz103-B39) 2002; 31
Challabathula (2023052516423494300_pcz103-B13) 2018; 227
Fern ndez-Mar n (2023052516423494300_pcz103-B22) 2010; 231
(2023052516423494300_pcz103-B56) 2016
Weissman (2023052516423494300_pcz103-B60) 2005; 71
Jones (2023052516423494300_pcz103-B34) 1985; 4
Foyer (2023052516423494300_pcz103-B24) 2001; 6
Kranner (2023052516423494300_pcz103-B41) 2005; 102
Kranner (2023052516423494300_pcz103-B37) 2002; 154
Kranner (2023052516423494300_pcz103-B40) 2005; 45
Banchi (2023052516423494300_pcz103-B6) 2018; 129
Amako (2023052516423494300_pcz103-B4) 1994; 35
Georgieva (2023052516423494300_pcz103-B28) 2017; 114
Schaedle (2023052516423494300_pcz103-B52) 1977; 59
Catal (2023052516423494300_pcz103-B11) 2010; 10
lvarez (2023052516423494300_pcz103-B2) 2015; 69
Inupakutika (2023052516423494300_pcz103-B33) 2016; 67
Silberstein (2023052516423494300_pcz103-B54) 1996; 28
References_xml – volume: 91
  start-page: 319
  year: 2016
  ident: 2023052516423494300_pcz103-B9
  article-title: New features of desiccation tolerance in the lichen photobiont Trebouxia gelatinosa are revealed by a transcriptomic approach
  publication-title: Plant Mol. Biol.
  doi: 10.1007/s11103-016-0468-5
– volume: 71
  start-page: 2121
  year: 2005
  ident: 2023052516423494300_pcz103-B59
  article-title: Rehydration of the lichen Ramalina lacera results in production of reactive oxygen species and nitric oxide and a decrease in antioxidants
  publication-title: Appl. Environ. Microbiol
  doi: 10.1128/AEM.71.4.2121-2129.2005
– volume: 107
  start-page: 109
  year: 2011
  ident: 2023052516423494300_pcz103-B15
  article-title: Oxidative stress induces distinct physiological responses in the two Trebouxia phycobionts of the lichen Ramalina farinacea
  publication-title: Ann. Bot
  doi: 10.1093/aob/mcq206
– volume: 26
  start-page: 1275
  year: 2003
  ident: 2023052516423494300_pcz103-B20
  article-title: An investigation into the role of light during desiccation of three angiosperm resurrection plants
  publication-title: Plant. Cell Environ.
  doi: 10.1046/j.0016-8025.2003.01052.x
– volume: 3
  start-page: RESEARCH0034
  year: 2002
  ident: 2023052516423494300_pcz103-B57
  article-title: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
  publication-title: Genome Biol
  doi: 10.1186/gb-2002-3-7-research0034
– volume: 18
  start-page: 1546
  year: 2016
  ident: 2023052516423494300_pcz103-B12
  article-title: Contrasting strategies used by lichen microalgae to cope with desiccation–rehydration stress revealed by metabolite profiling and cell wall analysis
  publication-title: Environ. Microbiol.
  doi: 10.1111/1462-2920.13249
– volume: 231
  start-page: 195
  year: 2009
  ident: 2023052516423494300_pcz103-B26
  article-title: Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms
  publication-title: Planta
  doi: 10.1007/s00425-009-1019-y
– volume: 30
  start-page: 1240
  year: 2007
  ident: 2023052516423494300_pcz103-B30
  article-title: Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives
  publication-title: Plant. Cell Environ.
  doi: 10.1111/j.1365-3040.2007.01704.x
– year: 2016
  ident: 2023052516423494300_pcz103-B56
– volume: 6
  start-page: 486
  year: 2001
  ident: 2023052516423494300_pcz103-B24
  article-title: The functions of inter- and intracellular glutathione transport systems in plants
  publication-title: Trends Plant Sci
  doi: 10.1016/S1360-1385(01)02086-6
– volume: 48
  start-page: 909
  year: 2010
  ident: 2023052516423494300_pcz103-B29
  article-title: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
  publication-title: Plant Physiol. Biochem
  doi: 10.1016/j.plaphy.2010.08.016
– start-page: 1
  volume-title: Plant Acclimation to Environmental Stress
  year: 2013
  ident: 2023052516423494300_pcz103-B23
– volume: 67
  start-page: 5933
  year: 2016
  ident: 2023052516423494300_pcz103-B33
  article-title: The evolution of reactive oxygen species metabolism
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erw382
– volume: 18
  start-page: 57
  year: 1986
  ident: 2023052516423494300_pcz103-B43
  article-title: Solorina Simensis and S. Saccata
  publication-title: Lichenologist
  doi: 10.1017/S0024282986000075
– volume: 44
  start-page: 301
  year: 1971
  ident: 2023052516423494300_pcz103-B61
  article-title: An improved procedure using ferricyanide for detecting catalase isozymes
  publication-title: Anal. Biochem
  doi: 10.1016/0003-2697(71)90375-7
– volume: 45
  start-page: 734
  year: 2005
  ident: 2023052516423494300_pcz103-B40
  article-title: A modulating role for antioxidants in desiccation tolerance
  publication-title: Integr. Comp. Biol.
  doi: 10.1093/icb/45.5.734
– volume: 42
  start-page: 267
  year: 1962
  ident: 2023052516423494300_pcz103-B7
  article-title: Some supplementary attributes in the classification of chlorococcum species
  publication-title: Arch. Mikrobiol.
  doi: 10.1007/BF00422045
– volume: 1797
  start-page: 331
  year: 2010
  ident: 2023052516423494300_pcz103-B35
  article-title: Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy
  publication-title: Bioenergetics
  doi: 10.1016/j.bbabio.2009.11.007
– volume: 35
  start-page: 454
  year: 2012
  ident: 2023052516423494300_pcz103-B47
  article-title: Glutathione in plants: an integrated overview
  publication-title: Plant. Cell Environ.
  doi: 10.1111/j.1365-3040.2011.02400.x
– volume: 227
  start-page: 84
  year: 2018
  ident: 2023052516423494300_pcz103-B13
  article-title: Protection of photosynthesis in desiccation-tolerant resurrection plants
  publication-title: J. Plant Physiol
  doi: 10.1016/j.jplph.2018.05.002
– volume: 102
  start-page: 3141
  year: 2005
  ident: 2023052516423494300_pcz103-B41
  article-title: Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0407716102
– volume: 160
  start-page: 167
  year: 2003
  ident: 2023052516423494300_pcz103-B42
  article-title: Biochemical traits of lichens differing in relative desiccation tolerance
  publication-title: New Phytol
  doi: 10.1046/j.1469-8137.2003.00852.x
– volume: 111
  start-page: 576
  year: 2008
  ident: 2023052516423494300_pcz103-B38
  article-title: Desiccation-tolerance in lichens: a review
  publication-title: Bryologist
  doi: 10.1639/0007-2745-111.4.576
– volume: 57
  start-page: 1377
  year: 2016
  ident: 2023052516423494300_pcz103-B44
  article-title: Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme?
  publication-title: Plant Cell Physiol
– volume: 57
  start-page: 1908
  year: 2016
  ident: 2023052516423494300_pcz103-B25
  article-title: The role of phospholipase d and MAPK signaling cascades in the adaption of lichen microalgae to desiccation: changes in membrane lipids and phosphoproteome
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcw111
– volume: 52
  start-page: 640
  year: 2007
  ident: 2023052516423494300_pcz103-B49
  article-title: Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression: and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death
  publication-title: Plant J
  doi: 10.1111/j.1365-313X.2007.03263.x
– volume: 169
  start-page: 1797
  year: 2012
  ident: 2023052516423494300_pcz103-B3
  article-title: Different strategies to achieve Pb-tolerance by the two Trebouxia algae coexisting in the lichen Ramalina farinacea
  publication-title: J. Plant. Physiol
  doi: 10.1016/j.jplph.2012.07.005
– volume: 35
  start-page: 497
  year: 1994
  ident: 2023052516423494300_pcz103-B4
  article-title: Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants
  publication-title: Plant Cell Physiol.
– volume: 28
  start-page: 367
  year: 1996
  ident: 2023052516423494300_pcz103-B54
  article-title: Comparative studies on Xanthoria parietina., a pollution resistant lichen: and Ramalina Duriaei: a sensitive species. II. evaluation of possible air pollution-protection mechanisms
  publication-title: Lichenologist
  doi: 10.1006/lich.1996.0034
– volume: 2017
  start-page: 7243973
  year: 2017
  ident: 2023052516423494300_pcz103-B63
  article-title: Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) family in response to various abiotic stresses
  publication-title: Int. J. Genomics
  doi: 10.1155/2017/7243973
– volume: 66
  start-page: 21
  year: 2015
  ident: 2023052516423494300_pcz103-B14
  article-title: Validation of candidate reference genes for qRT-PCR studies in symbiotic and non-symbiotic Casuarina glauca Sieb. ex Spreng. under salinity conditions
  publication-title: Symbiosis
  doi: 10.1007/s13199-015-0330-6
– volume: 41
  start-page: 571
  year: 2003
  ident: 2023052516423494300_pcz103-B36
  article-title: Moderately elevated temperature eliminates resistance of rice plants with enhanced expression of glutathione reductase to intensive photooxidative stress
  publication-title: Photosynthetica
  doi: 10.1023/B:PHOT.0000027522.35486.f6
– volume: 31
  start-page: 113
  year: 2001
  ident: 2023052516423494300_pcz103-B45
  article-title: The effect of desiccation on the activities of antioxidant enzymes in lichens from habitats of contrasting water status
  publication-title: Symbiosis
– volume: 70
  start-page: 689
  year: 2013
  ident: 2023052516423494300_pcz103-B27
  article-title: Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis
  publication-title: Cell. Mol. Life Sci.
  doi: 10.1007/s00018-012-1155-6
– volume: 1817
  start-page: 1314
  year: 2012
  ident: 2023052516423494300_pcz103-B46
  article-title: Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/j.bbabio.2012.02.036
– volume: 142
  start-page: 65
  year: 2011
  ident: 2023052516423494300_pcz103-B31
  article-title: Photoprotection of reaction centers: thermal dissipation of absorbed light energy vs charge separation in lichens
  publication-title: Physiol. Plant
  doi: 10.1111/j.1399-3054.2010.01417.x
– volume: 10
  start-page: 297
  year: 2010
  ident: 2023052516423494300_pcz103-B11
  article-title: Fungal-associated NO is involved in the regulation of oxidative stress during rehydration in lichen symbiosis
  publication-title: BMC Microbiol.
  doi: 10.1186/1471-2180-10-297
– volume: 4
  start-page: 482
  year: 2013
  ident: 2023052516423494300_pcz103-B17
  article-title: Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis
  publication-title: Front. Plant Sci
  doi: 10.3389/fpls.2013.00482
– volume: 7
  start-page: 1279
  year: 2016
  ident: 2023052516423494300_pcz103-B21
  article-title: The SOD gene family in tomato: identification, phylogenetic relationships, and expression patterns
  publication-title: Front. Plant Sci
  doi: 10.3389/fpls.2016.01279
– volume: 9
  start-page: e110630
  year: 2014
  ident: 2023052516423494300_pcz103-B32
  article-title: Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0110630
– volume: 129
  start-page: 189
  year: 2018
  ident: 2023052516423494300_pcz103-B6
  article-title: Relation between water status and desiccation-affected genes in the lichen photobiont Trebouxia gelatinosa
  publication-title: Plant Physiol. Biochem
  doi: 10.1016/j.plaphy.2018.06.004
– volume: 13
  start-page: 806
  year: 2011
  ident: 2023052516423494300_pcz103-B10
  article-title: Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition?
  publication-title: Environ. Microbiol
  doi: 10.1111/j.1462-2920.2010.02386.x
– volume: 231
  start-page: 1335
  year: 2010
  ident: 2023052516423494300_pcz103-B22
  article-title: Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria
  publication-title: Planta
  doi: 10.1007/s00425-010-1129-6
– volume: 15
  start-page: 351
  year: 2014
  ident: 2023052516423494300_pcz103-B51
  article-title: Regulation of photosynthetic electron transport and photoinhibition
  publication-title: Curr. Protein Pept. Sci.
  doi: 10.2174/1389203715666140327105143
– volume: 53
  start-page: 1305
  year: 2002
  ident: 2023052516423494300_pcz103-B53
  article-title: Regulation and function of ascorbate peroxidase isoenzymes
  publication-title: J. Exp. Bot.
  doi: 10.1093/jexbot/53.372.1305
– volume: 114
  start-page: 51
  year: 2017
  ident: 2023052516423494300_pcz103-B28
  article-title: Antioxidant defense during desiccation of the resurrection plant Haberlea rhodopensis
  publication-title: Plant Physiol. Biochem
  doi: 10.1016/j.plaphy.2017.02.021
– volume: 71
  start-page: 6508
  year: 2005
  ident: 2023052516423494300_pcz103-B60
  article-title: Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration
  publication-title: Appl. Environ. Microbiol
  doi: 10.1128/AEM.71.11.6508-6514.2005
– volume: 39
  start-page: 20
  year: 2016
  ident: 2023052516423494300_pcz103-B16
  article-title: Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast?
  publication-title: Mol. Cells
  doi: 10.14348/molcells.2016.2324
– start-page: 65
  volume-title: Advances in Photosynthesis and Respiration. Chlorophyll a Fluorescence: A Signature of Photosynthesis
  year: 2004
  ident: 2023052516423494300_pcz103-B5
  doi: 10.1007/978-1-4020-3218-9_3
– volume: 151
  start-page: 29
  year: 2000
  ident: 2023052516423494300_pcz103-B18
  article-title: A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species
  publication-title: Plant Ecol
  doi: 10.1023/A:1026534305831
– volume: 154
  start-page: 451
  year: 2002
  ident: 2023052516423494300_pcz103-B37
  article-title: Glutathione status correlates with different degrees of desiccation tolerance in three lichens
  publication-title: New Phytol.
  doi: 10.1046/j.1469-8137.2002.00376.x
– volume: 4
  start-page: 2411
  year: 1985
  ident: 2023052516423494300_pcz103-B34
  article-title: High level expression of introduced chimaeric genes in regenerated transformed plants
  publication-title: EMBO J
  doi: 10.1002/j.1460-2075.1985.tb03949.x
– volume: 9
  start-page: 565
  year: 2007
  ident: 2023052516423494300_pcz103-B50
  article-title: Novel insight into the regulation of GSH biosynthesis in higher plants
  publication-title: Plant Biol. (Stuttg)
  doi: 10.1055/s-2007-965580
– volume: 23
  start-page: 995
  year: 2011
  ident: 2023052516423494300_pcz103-B58
  article-title: Cloning and expression of isoenzymes of superoxide dismutase in Haematococcus pluvialis (Chlorophyceae) under oxidative stress
  publication-title: J. Appl. Phycol.
  doi: 10.1007/s10811-010-9631-6
– volume: 72
  start-page: 983
  year: 2012
  ident: 2023052516423494300_pcz103-B62
  article-title: Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait
  publication-title: Plant J
  doi: 10.1111/tpj.12008
– volume: 24
  start-page: 193
  year: 1998
  ident: 2023052516423494300_pcz103-B48
  article-title: ‘To dryness and beyond’—preparation for the dried state and rehydration in vegetative desiccation-tolerant plants
  publication-title: Plant Growth Regul
  doi: 10.1023/A:1005863015130
– volume: 53
  start-page: 1331
  year: 2002
  ident: 2023052516423494300_pcz103-B1
  article-title: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants
  publication-title: J. Exp. Biol
– volume: 59
  start-page: 1011
  year: 1977
  ident: 2023052516423494300_pcz103-B52
  article-title: Chloroplast glutathione reductase
  publication-title: Plant Physiol
  doi: 10.1104/pp.59.5.1011
– volume: 31
  start-page: 13
  year: 2002
  ident: 2023052516423494300_pcz103-B39
  article-title: Revival of a resurrection plant correlates with its antioxidant status
  publication-title: Plant J.
  doi: 10.1046/j.1365-313X.2002.01329.x
– volume: 72
  start-page: 248
  year: 1976
  ident: 2023052516423494300_pcz103-B8
  article-title: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
  publication-title: Anal. Biochem
  doi: 10.1016/0003-2697(76)90527-3
– volume: 69
  start-page: 698
  year: 2015
  ident: 2023052516423494300_pcz103-B2
  article-title: Lichen rehydration in heavy metal-polluted environments: Pb modulates the oxidative response of both Ramalina farinacea thalli and its isolated microalgae
  publication-title: Microb. Ecol.
  doi: 10.1007/s00248-014-0524-0
– volume: 14
  start-page: 340
  year: 2011
  ident: 2023052516423494300_pcz103-B19
  article-title: Programming desiccation-tolerance: from plants to seeds to resurrection plants
  publication-title: Curr. Opin. Plant Biol
  doi: 10.1016/j.pbi.2011.03.018
– volume: 221
  start-page: 1197
  year: 2019
  ident: 2023052516423494300_pcz103-B55
  article-title: Hydrogen peroxide metabolism and functions in plants
  publication-title: New Phytol.
  doi: 10.1111/nph.15488
SSID ssj0007830
Score 2.3838885
Snippet Oxidative stress is a crucial challenge for lichens exposed to cyclic desiccation and rehydration (D/R). However, strategies to overcome this potential stress...
SourceID proquest
pubmed
crossref
SourceType Aggregation Database
Index Database
Enrichment Source
StartPage 1880
SubjectTerms Antioxidants - metabolism
Desiccation
Lichens - metabolism
Microalgae - metabolism
Oxidative Stress - physiology
Superoxide Dismutase - metabolism
Title Tolerance to Cyclic Desiccation in Lichen Microalgae is Related to Habitat Preference and Involves Specific Priming of the Antioxidant System
URI https://www.ncbi.nlm.nih.gov/pubmed/31127294
https://www.proquest.com/docview/2232087577
Volume 60
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Zb9NAEF6FAhIvFZSr5dAieEGR28TexPZjKEc4ylMr9c3as4oU2VEOieQ_8Lf4Xcx4dh2XFqnwsopsr614Ps-1384w9sYZl-ZGQlgy0DYSSpkoGwgV5VqIWFls9YB7h0--D8dn4sv54LzT-dViLa2W6lBvrt1X8j9ShWMgV9wl-w-SbW4KB-A3yBdGkDCMN5NxNbXzmvMPHuTxWmPBaggkJ5rycJjL-IZUzxLZ8fMKt21Y7GBeM-DA04RZY6lwlxlSMULFWWIIg9rCgrR1f3qH_Pm6_9dF4BSMkCX5Y2JAML7qedvNxVZIRF3HhQFKn1zK34_9cseo9nIbdvEnuYCQWAaPWk8WumrOVeWmO7WbaIzrDb5c8ImcdxvDYuy0i2spdfYXQgSf6fU5DdxGlYWchtfTCXJiqZnLoSXVDGY0yntUWjjobupF4DGatRQxlplrGfV-Rj3BrhgMKqY107N63PR7ydYwBjLAH_ayYTHS-n1SwOyC5t5it2MIV7CTxvvPXxuPIM0SXx6U_lUok5snRzD3iOZedoz-Eu3UXs_pfbbrwxU-Iuw9YB1b7rG71MB0vcfuvKsguFg_ZD8bKPJlxQmKvAVFPik5QZFvocgnC-6hiLM8FPkWihwQxAMUeYAi91DkleMARd6CIicoPmJnHz-cHo8j3-kj0hCxL0EzxM70EyVSsALO2kwblUgDwQXAybg-hCFaZ6mRUkihrXMqTntDlSlwRjOt4-Qx2ymr0j5lHF61VTrVcFIKY4bK9TLrpBBDY_PBIN1nb8NrLrQvg4_dWKbFVXHus9fNtTMq_nLtVa-CtArQzfhdydJWq0UBrndcd4yApz4hMTb3SSDQgcBWHNzoGc_Yve138pztLOcr-wK84aV6WUPtN9REv3c
linkProvider Flying Publisher
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Tolerance+to+Cyclic+Desiccation+in+Lichen+Microalgae+is+Related+to+Habitat+Preference+and+Involves+Specific+Priming+of+the+Antioxidant+System&rft.jtitle=Plant+and+cell+physiology&rft.au=Hell%2C+Aline+F&rft.au=Gasulla%2C+Francisco&rft.au=Gonz+lez-Hourcade%2C+Mar+a&rft.au=del+Campo%2C+Eva+M&rft.date=2019-08-01&rft.issn=0032-0781&rft.eissn=1471-9053&rft.volume=60&rft.issue=8&rft.spage=1880&rft.epage=1891&rft_id=info:doi/10.1093%2Fpcp%2Fpcz103&rft.externalDBID=n%2Fa&rft.externalDocID=10_1093_pcp_pcz103
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0032-0781&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0032-0781&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0032-0781&client=summon