Yellow Canopy Syndrome in sugarcane is associated with shifts in the rhizosphere soil metagenome but not with overall soil microbial function

TitleYellow Canopy Syndrome in sugarcane is associated with shifts in the rhizosphere soil metagenome but not with overall soil microbial function
Publication TypeJournal Article
Year of Publication2018
AuthorsHamonts K., Trivedi P., Grinyer J., Holford P., Drigo B., Anderson I.A, Singh B.K
JournalSoil Biology and Biochemistry
Volume125
Pagination275-285
Date PublishedOct
Type of ArticleArticle
ISBN Number0038-0717
Accession NumberWOS:000444660400030
KeywordsAgriculture, bacterial communities, canopy syndrome, disease, diversity, greengenes, healthy, identification, Microbial functions, plant, Rhizosphere soil microbiome, root, sensitivity, sequences, sugarcane, Yellow
Abstract

The Australian sugarcane industry is facing a new threat of the currently undiagnosed Yellow Canopy Syndrome (YCS). Here, we investigated if YCS is linked to detrimental shifts in soil microbial function and/or altered physico-chemical soil properties. We examined changes in rhizosphere soil microbial assemblages, functional gene profiles and microbial activity associated with YCS development. Shifts in soil bacterial and fungal community assemblages with YCS appeared variety-specific with limited consistent trends emerging. However, significant, consistent shifts in the rhizosphere soil metagenome with YCS were found, suggesting that YCS incidence might be linked to changes in specific soil microbial functions. Functional gene categories involved in prokaryotic immune response and in metabolism of compounds present in root exudates were consistently detected in higher abundance in the rhizosphere of YCS-affected plants, while gene categories involved in DNA, RNA and protein processing were consistently less abundant. Soil nutrient status (C, N), extracellular enzyme activity and substrate-induced respiration either did not significantly differ between affected and healthy fields of three sugarcane varieties, or showed inconsistent trends with variety. Altogether, our results did not show a direct link between soil microbial richness, overall soil microbial activity, soil nutrient status and YCS incidence. However, rhizosphere microbial communities responded consistently to YCS incidence by enrichment of genes encoding functions involved in defence against pathogens and root exudate metabolism which may have potential implications for the future development of diagnostic tools and an effective management practice to minimise impact of YCS on farm productivity.

Short TitleSoil Biol. Biochem.Soil Biol. Biochem.
Alternate JournalSoil Biol. Biochem.
stdClass Object
(
    [vid] => 508
    [uid] => 1
    [title] => Yellow Canopy Syndrome in sugarcane is associated with shifts in the rhizosphere soil metagenome but not with overall soil microbial function
    [log] => 
    [status] => 1
    [comment] => 0
    [promote] => 1
    [sticky] => 0
    [nid] => 455
    [type] => biblio
    [language] => und
    [created] => 1584009522
    [changed] => 1584009522
    [tnid] => 0
    [translate] => 0
    [revision_timestamp] => 1584009522
    [revision_uid] => 11
    [biblio_type] => 102
    [biblio_number] => 
    [biblio_other_number] => 
    [biblio_sort_title] => Yellow Canopy Syndrome in sugarcane is associated with shifts in
    [biblio_secondary_title] => Soil Biology and Biochemistry
    [biblio_tertiary_title] => 
    [biblio_edition] => 
    [biblio_publisher] => 
    [biblio_place_published] => 
    [biblio_year] => 2018
    [biblio_volume] => 125
    [biblio_pages] => 275-285
    [biblio_date] => Oct
    [biblio_isbn] => 0038-0717
    [biblio_lang] => English
    [biblio_abst_e] => The Australian sugarcane industry is facing a new threat of the currently undiagnosed Yellow Canopy Syndrome (YCS). Here, we investigated if YCS is linked to detrimental shifts in soil microbial function and/or altered physico-chemical soil properties. We examined changes in rhizosphere soil microbial assemblages, functional gene profiles and microbial activity associated with YCS development. Shifts in soil bacterial and fungal community assemblages with YCS appeared variety-specific with limited consistent trends emerging. However, significant, consistent shifts in the rhizosphere soil metagenome with YCS were found, suggesting that YCS incidence might be linked to changes in specific soil microbial functions. Functional gene categories involved in prokaryotic immune response and in metabolism of compounds present in root exudates were consistently detected in higher abundance in the rhizosphere of YCS-affected plants, while gene categories involved in DNA, RNA and protein processing were consistently less abundant. Soil nutrient status (C, N), extracellular enzyme activity and substrate-induced respiration either did not significantly differ between affected and healthy fields of three sugarcane varieties, or showed inconsistent trends with variety. Altogether, our results did not show a direct link between soil microbial richness, overall soil microbial activity, soil nutrient status and YCS incidence. However, rhizosphere microbial communities responded consistently to YCS incidence by enrichment of genes encoding functions involved in defence against pathogens and root exudate metabolism which may have potential implications for the future development of diagnostic tools and an effective management practice to minimise impact of YCS on farm productivity.
    [biblio_abst_f] => 
    [biblio_full_text] => 0
    [biblio_url] => 
    [biblio_issue] => 
    [biblio_type_of_work] => Article
    [biblio_accession_number] => WOS:000444660400030
    [biblio_call_number] => 
    [biblio_notes] => ISI Document Delivery No.: GT6WA
Times Cited: 1
Cited Reference Count: 70
Cited References:
Anderson MJ, 1998, AUST J ECOL, V23, P158, DOI 10.1111/j.1442-9993.1998.tb00713.x
Anderson MJ, 2001, AUSTRAL ECOL, V26, P32, DOI 10.1111/j.1442-9993.2001.01070.pp.x
Andrews S, 2010, FASTQC QUALITY CONTR
Araujo WL, 2002, APPL ENVIRON MICROB, V68, P4906, DOI 10.1128/AEM.68.10.4906-4914.2002
BENJAMINI Y, 1995, J R STAT SOC B, V57, P289
Blakemore L. C., 1987, SCI REPORT, V80
Bulgarelli D, 2015, CELL HOST MICROBE, V17, P392, DOI 10.1016/j.chom.2015.01.011
Busby PE, 2017, PLOS BIOL, V15, DOI 10.1371/journal.pbio.2001793
Campbell CD, 2003, APPL ENVIRON MICROB, V69, P3593, DOI 10.1128/AEM.69.6.3593-3599.2003
Campbell CD, 1997, J MICROBIOL METH, V30, P33, DOI 10.1016/S0167-7012(97)00041-9
CLARKE KR, 1993, AUST J ECOL, V18, P117, DOI 10.1111/j.1442-9993.1993.tb00438.x
Clarke KR, 2001, CHANGE MARINE COMMUN
Colin Y, 2017, SCI REP-UK, V7, DOI 10.1038/s41598-017-07639-1
Dakora F.D., 2002, FOOD SECURITY NUTR S, P201, DOI DOI 10.1007/978-94-017-1570-6_23
DeSantis TZ, 2006, APPL ENVIRON MICROB, V72, P5069, DOI 10.1128/AEM.03006-05
DUNN OJ, 1964, TECHNOMETRICS, V6, P241, DOI 10.2307/1266041
Edgar RC, 2013, NAT METHODS, V10, P996, DOI [10.1038/NMETH.2604, 10.1038/nmeth.2604]
Edgar RC, 2011, BIOINFORMATICS, V27, P2194, DOI 10.1093/bioinformatics/btr381
Filion M, 2004, APPL ENVIRON MICROB, V70, P3541, DOI 10.1128/AEM.70.6.3541-3551.2004
Fox J, 2011, R COMPANION APPL REG
Gardener BBM, 2001, APPL ENVIRON MICROB, V67, P4414, DOI 10.1128/AEM.67.10.4414-4425.2001
Garside AL, 2005, INT SUGAR J, V107, P16
GOWER JC, 1966, BIOMETRIKA, V53, P325, DOI 10.1093/biomet/53.3-4.325
Hamonts K, 2018, ENVIRON MICROBIOL, V20, P124, DOI 10.1111/1462-2920.14031
Hardoim PR, 2015, MICROBIOL MOL BIOL R, V79, P293, DOI 10.1128/MMBR.00050-14
Herlemann DPR, 2011, ISME J, V5, P1571, DOI 10.1038/ismej.2011.41
Hollander M, 1973, NONPARAMETRIC STAT M, P115
Hothorn T, 2008, BIOMETRICAL J, V50, P346, DOI 10.1002/bimj.200810425
Houston K, 2016, FRONT PLANT SCI, V7, DOI 10.3389/fpls.2016.00984
Ihrmark K, 2012, FEMS MICROBIOL ECOL, V82, P666, DOI 10.1111/j.1574-6941.2012.01437.x
Jones DL, 2009, PLANT SOIL, V321, P5, DOI 10.1007/s11104-009-9925-0
Kamilova F, 2006, MOL PLANT MICROBE IN, V19, P250, DOI 10.1094/MPMI-19-0250
Kibblewhite MG, 2008, PHILOS T R SOC B, V363, P685, DOI 10.1098/rstb.2007.2178
Koljalg U, 2013, MOL ECOL, V22, P5271, DOI 10.1111/mec.12481
Lang JM, 2017, PHYTOPATHOLOGY, V107, P1312, DOI 10.1094/PHYTO-05-17-0168-R
Lenth RV, 2016, J STAT SOFTW, V69, P1, DOI 10.18637/jss.v069.i01
Lueders T, 2004, ENVIRON MICROBIOL, V6, P73, DOI 10.1046/j.1462-2920.2003.00536.x
Lueders T, 2004, APPL ENVIRON MICROB, V70, P5778, DOI 10.1128/AEM.70.10.5778-5786.2004
Magoc T, 2011, BIOINFORMATICS, V27, P2957, DOI 10.1093/bioinformatics/btr507
Makarova KS, 2013, NUCLEIC ACIDS RES, V41, P4360, DOI 10.1093/nar/gkt157
Marquardt A, 2016, FUNCT PLANT BIOL, V43, P523, DOI 10.1071/FP15335
Matilla MA, 2010, ENV MICROBIOL REP, V2, P381, DOI 10.1111/j.1758-2229.2009.00091.x
McArdle BH, 2001, ECOLOGY, V82, P290, DOI 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
McDonald D, 2012, ISME J, V6, P610, DOI 10.1038/ismej.2011.139
Mendes R, 2011, SCIENCE, V332, P1097, DOI 10.1126/science.1203980
Meyer F, 2008, BMC BIOINFORMATICS, V9, DOI 10.1186/1471-2105-9-386
Overbeek R, 2005, NUCLEIC ACIDS RES, V33, P5691, DOI 10.1093/nar/gki866
Parks DH, 2010, BIOINFORMATICS, V26, P715, DOI 10.1093/bioinformatics/btq041
Phillips DA, 2004, PLANT PHYSIOL, V136, P2887, DOI 10.1104/pp.104.044222
Pinton R., 2007, RHIZOSPHERE BIOCH OR, P23, DOI DOI 10.1201/9781420005585.CH2
Ranf S, 2016, MOL PLANT PATHOL, V17, P1165, DOI 10.1111/mpp.12452
Ranf S, 2016, PLOS PATHOG, V12, DOI 10.1371/journal.ppat.1005596
Reiter B, 2002, APPL ENVIRON MICROB, V68, P2261, DOI 10.1128/AEM.68.5.2261-2268.2002
Sagaram US, 2009, APPL ENVIRON MICROB, V75, P1566, DOI 10.1128/AEM.02404-08
Saiya-Cork KR, 2002, SOIL BIOL BIOCHEM, V34, P1309, DOI 10.1016/S0038-0717(02)00074-3
Schloss PD, 2009, APPL ENVIRON MICROB, V75, P7537, DOI 10.1128/AEM.01541-09
Schmalenberger A, 2008, ENVIRON MICROBIOL, V10, P1486, DOI 10.1111/j.1462-2920.2007.01564.x
Singh BK, 2017, MICROB BIOTECHNOL, V10, P50, DOI 10.1111/1751-7915.12592
Sinsabaugh RL, 2003, APPL SOIL ECOL, V24, P263, DOI 10.1016/S0929-1393(03)00002-7
Trivedi P, 2017, SOIL BIOL BIOCHEM, V111, P10, DOI 10.1016/j.soilbio.2017.03.013
Trivedi P, 2016, FRONT PLANT SCI, V7, DOI 10.3389/fpls.2016.00990
Trivedi P, 2012, ISME J, V6, P363, DOI 10.1038/ismej.2011.100
Trivedi P, 2011, MICROB ECOL, V62, P324, DOI 10.1007/s00248-011-9822-y
Trivedi P, 2010, APPL ENVIRON MICROB, V76, P3427, DOI 10.1128/AEM.02901-09
Tyler HL, 2009, MOL PLANT MICROBE IN, V22, P1624, DOI 10.1094/MPMI-22-12-1624
Vujanovic V, 2007, MICROB ECOL, V54, P672, DOI 10.1007/s00248-007-9226-1
Wang N, 2013, PHYTOPATHOLOGY, V103, P652, DOI 10.1094/PHYTO-12-12-0331-RVW
Wang Q, 2007, APPL ENVIRON MICROB, V73, P5261, DOI 10.1128/AEM.00062-07
Yang CH, 2001, FEMS MICROBIOL ECOL, V35, P129, DOI 10.1111/j.1574-6941.2001.tb00796.x
Zhu YG, 2016, SCI BULL, V61, P1052, DOI 10.1007/s11434-016-1112-0
Hamonts, Kelly Trivedi, Pankaj Grinyer, Jasmine Holford, Paul Drigo, Barbara Anderson, Ian A. Singh, Brajesh K.
Singh, Brajesh/R-6321-2019
Singh, Brajesh/0000-0003-4413-4185; Drigo, Barbara/0000-0002-3301-0470
Sugar Research Australia (YCS-Integrated Research Program) [2014/082]; Queensland government; Western Sydney University; Australian Research CouncilAustralian Research Council [DP170104634]
This study was funded by Sugar Research Australia (YCS-Integrated Research Program project 2014/082), the Queensland government and Western Sydney University. We thank Lawrence Di Bella for assistance in identifying sampling sites and Anshu Garg, Melissa Martin, Krista Plett and Smriti Rayu for technical support. BKS work on plant-microbial interaction is funded by Australian Research Council (DP170104634).
1
10
37
Pergamon-elsevier science ltd
Oxford [biblio_custom1] => [biblio_custom2] => [biblio_custom3] => [biblio_custom4] => [biblio_custom5] => [biblio_custom6] => [biblio_custom7] => [biblio_research_notes] => [biblio_number_of_volumes] => [biblio_short_title] => Soil Biol. Biochem.Soil Biol. Biochem. [biblio_alternate_title] => Soil Biol. Biochem. [biblio_original_publication] => [biblio_reprint_edition] => [biblio_translated_title] => [biblio_section] => [biblio_citekey] => 455 [biblio_coins] => [biblio_doi] => [biblio_issn] => [biblio_auth_address] => [Hamonts, Kelly; Grinyer, Jasmine; Anderson, Ian A.; Singh, Brajesh K.] Western Sydney Univ, Hawkesbury Inst Environm, Penrith, NSW, Australia. [Trivedi, Pankaj] Colorado State Univ, Dept Bioagr Sci & Pest Management, Ft Collins, CO 80523 USA. [Holford, Paul] Western Sydney Univ, Sch Sci & Hlth, Penrith, NSW, Australia. [Drigo, Barbara; Singh, Brajesh K.] Western Sydney Univ, Global Ctr Land Based Innovat, Penrith, NSW, Australia.
Hamonts, K; Singh, BK (reprint author), Western Sydney Univ, Hawkesbury Inst Environm, Penrith, NSW, Australia.; Trivedi, P (reprint author), Colorado State Univ, Dept Bioagr Sci & Pest Management, Ft Collins, CO 80523 USA.
K.Hamonts@westernsydney.edu.au; Pankaj.Trivedi@colostate.edu; b.singh@westernsydney.edu.au [biblio_remote_db_name] => [biblio_remote_db_provider] => [biblio_label] => [biblio_access_date] => [biblio_refereed] => [biblio_md5] => baf1eb19a93e2c71049512c84745c5a2 [biblio_formats] => Array ( [biblio_abst_e] => full_html [biblio_abst_f] => full_html [biblio_notes] => full_html [biblio_research_notes] => full_html [biblio_custom1] => full_html [biblio_custom2] => full_html [biblio_custom3] => full_html [biblio_custom4] => full_html [biblio_custom5] => full_html [biblio_custom6] => full_html [biblio_custom7] => full_html [biblio_coins] => full_html [biblio_auth_address] => full_html ) [biblio_type_name] => Journal Article [biblio_contributors] => Array ( [0] => Array ( [nid] => 455 [vid] => 508 [cid] => 916 [auth_type] => 1 [auth_category] => 1 [rank] => 0 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Hamonts, K. [lastname] => Hamonts [firstname] => K. [prefix] => [suffix] => [initials] => [affiliation] => [literal] => 0 [md5] => 46af4cb54d76c344f039310023987d35 ) [1] => Array ( [nid] => 455 [vid] => 508 [cid] => 746 [auth_type] => 1 [auth_category] => 1 [rank] => 1 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Trivedi, P. [lastname] => Trivedi [firstname] => P. [prefix] => [suffix] => [initials] => [affiliation] => [literal] => 0 [md5] => 7727bb51f9440fb562d5977792ccd193 ) [2] => Array ( [nid] => 455 [vid] => 508 [cid] => 917 [auth_type] => 1 [auth_category] => 1 [rank] => 2 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Grinyer, J. [lastname] => Grinyer [firstname] => J. [prefix] => [suffix] => [initials] => [affiliation] => [literal] => 0 [md5] => ca118f7859fdf55779d9fc7921e9d15d ) [3] => Array ( [nid] => 455 [vid] => 508 [cid] => 918 [auth_type] => 1 [auth_category] => 1 [rank] => 3 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Holford, P. [lastname] => Holford [firstname] => P. [prefix] => [suffix] => [initials] => [affiliation] => [literal] => 0 [md5] => 7248f1094540af1be1b8d9b40f31ae25 ) [4] => Array ( [nid] => 455 [vid] => 508 [cid] => 919 [auth_type] => 1 [auth_category] => 1 [rank] => 4 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Drigo, B. [lastname] => Drigo [firstname] => B. [prefix] => [suffix] => [initials] => [affiliation] => [literal] => 0 [md5] => bef5fcd7447eb3c3ad1044871624afeb ) [5] => Array ( [nid] => 455 [vid] => 508 [cid] => 920 [auth_type] => 1 [auth_category] => 1 [rank] => 5 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Anderson, I. A. [lastname] => Anderson [firstname] => I. [prefix] => [suffix] => [initials] => A. [affiliation] => [literal] => 0 [md5] => 0b9b282d3816427e8b8274ec82ae5d2a ) [6] => Array ( [nid] => 455 [vid] => 508 [cid] => 167 [auth_type] => 1 [auth_category] => 1 [rank] => 6 [merge_cid] => 0 [aka] => 0 [alt_form] => 0 [drupal_uid] => [name] => Singh, B. K. [lastname] => Singh [firstname] => B. [prefix] => [suffix] => [initials] => K. [affiliation] => [literal] => 0 [md5] => b59c9500754b536a90eabcf3ebaa13ea ) ) [biblio_keywords] => Array ( [421] => Agriculture [263] => bacterial communities [1292] => canopy syndrome [1293] => disease [132] => diversity [1295] => greengenes [1297] => healthy [1155] => identification [1290] => Microbial functions [365] => plant [1289] => Rhizosphere soil microbiome [864] => root [1294] => sensitivity [1296] => sequences [377] => sugarcane [1291] => Yellow ) [body] => Array ( ) [rdf_mapping] => Array ( [rdftype] => Array ( [0] => sioc:Item [1] => foaf:Document ) [title] => Array ( [predicates] => Array ( [0] => dc:title ) ) [created] => Array ( [predicates] => Array ( [0] => dc:date [1] => dc:created ) [datatype] => xsd:dateTime [callback] => date_iso8601 ) [changed] => Array ( [predicates] => Array ( [0] => dc:modified ) [datatype] => xsd:dateTime [callback] => date_iso8601 ) [body] => Array ( [predicates] => Array ( [0] => content:encoded ) ) [uid] => Array ( [predicates] => Array ( [0] => sioc:has_creator ) [type] => rel ) [name] => Array ( [predicates] => Array ( [0] => foaf:name ) ) [comment_count] => Array ( [predicates] => Array ( [0] => sioc:num_replies ) [datatype] => xsd:integer ) [last_activity] => Array ( [predicates] => Array ( [0] => sioc:last_activity_date ) [datatype] => xsd:dateTime [callback] => date_iso8601 ) ) [name] => admin [picture] => 0 [data] => a:14:{s:7:"overlay";i:0;s:16:"ckeditor_default";s:1:"t";s:20:"ckeditor_show_toggle";s:1:"t";s:14:"ckeditor_width";s:4:"100%";s:13:"ckeditor_lang";s:2:"en";s:18:"ckeditor_auto_lang";s:1:"t";s:19:"biblio_show_profile";i:0;s:19:"biblio_my_pubs_menu";i:0;s:21:"biblio_contributor_id";s:1:"0";s:22:"biblio_id_change_count";s:1:"0";s:17:"biblio_user_style";s:6:"system";s:18:"biblio_baseopenurl";s:0:"";s:18:"biblio_openurl_sid";s:0:"";s:19:"biblio_crossref_pid";s:0:"";} [entity_view_prepared] => 1 )