TY - JOUR

T1 - Constitutive expression of apple endo-POLYGALACTURONASE1 in fruit induces early maturation, alters skin structure and accelerates softening

AU - Gunaseelan, Kularajathevan

AU - Schröder, Roswitha

AU - Rebstock, Ria

AU - Ninan, Annu S.

AU - Deng, Cecilia

AU - Khanal, Bishnu P.

AU - Favre, Laurie

AU - Tomes, Sumathi

AU - Dragulescu, Monica A.

AU - O'Donoghue, Erin M.

AU - Hallett, Ian C.

AU - Schaffer, Robert J.

AU - Knoche, Moritz

AU - Brummell, David A.

AU - Atkinson, Ross G.

N1 - Funding Information: KG obtained the physiological data. KG, RS, AN and EOD carried out biochemical, molecular and cell wall analyses. CD and LF analysed the transcriptomic data. ST and MD made and cared for the transgenic plants. BK and MK conducted transpiration assays. RR and IH undertook the immunolabelling and microscopy. RS, RJS, MK, DB and RA designed the research, analysed the data and wrote the paper. This work was funded by the New Zealand Ministry of Business, Innovation and Employment and internal Plant & Food Research funding.

PY - 2024/2/26

Y1 - 2024/2/26

N2 - During fruit ripening, polygalacturonases (PGs) are key contributors to the softening process in many species. Apple is a crisp fruit that normally exhibits only minor changes to cell walls and limited fruit softening. Here, we explore the effects of PG overexpression during fruit development using transgenic apple lines overexpressing the ripening-related endo-POLYGALACTURONASE1 gene. MdPG1-overexpressing (PGox) fruit displayed early maturation/ripening with black seeds, conversion of starch to sugars and ethylene production occurring by 80 days after pollination (DAP). PGox fruit exhibited a striking, white-skinned phenotype that was evident from 60 DAP and most likely resulted from increased air spaces and separation of cells in the hypodermis due to degradation of the middle lamellae. Irregularities in the integrity of the epidermis and cuticle were also observed. By 120 DAP, PGox fruit cracked and showed lenticel-associated russeting. Increased cuticular permeability was associated with microcracks in the cuticle around lenticels and was correlated with reduced cortical firmness at all time points and extensive post-harvest water loss from the fruit, resulting in premature shrivelling. Transcriptomic analysis suggested that early maturation was associated with upregulation of genes involved in stress responses, and overexpression of MdPG1 also altered the expression of genes involved in cell wall metabolism (e.g. β-galactosidase, MD15G1221000) and ethylene biosynthesis (e.g. ACC synthase, MD14G1111500). The results show that upregulation of PG not only has dramatic effects on the structure of the fruit outer cell layers, indirectly affecting water status and turgor, but also has unexpected consequences for fruit development.

AB - During fruit ripening, polygalacturonases (PGs) are key contributors to the softening process in many species. Apple is a crisp fruit that normally exhibits only minor changes to cell walls and limited fruit softening. Here, we explore the effects of PG overexpression during fruit development using transgenic apple lines overexpressing the ripening-related endo-POLYGALACTURONASE1 gene. MdPG1-overexpressing (PGox) fruit displayed early maturation/ripening with black seeds, conversion of starch to sugars and ethylene production occurring by 80 days after pollination (DAP). PGox fruit exhibited a striking, white-skinned phenotype that was evident from 60 DAP and most likely resulted from increased air spaces and separation of cells in the hypodermis due to degradation of the middle lamellae. Irregularities in the integrity of the epidermis and cuticle were also observed. By 120 DAP, PGox fruit cracked and showed lenticel-associated russeting. Increased cuticular permeability was associated with microcracks in the cuticle around lenticels and was correlated with reduced cortical firmness at all time points and extensive post-harvest water loss from the fruit, resulting in premature shrivelling. Transcriptomic analysis suggested that early maturation was associated with upregulation of genes involved in stress responses, and overexpression of MdPG1 also altered the expression of genes involved in cell wall metabolism (e.g. β-galactosidase, MD15G1221000) and ethylene biosynthesis (e.g. ACC synthase, MD14G1111500). The results show that upregulation of PG not only has dramatic effects on the structure of the fruit outer cell layers, indirectly affecting water status and turgor, but also has unexpected consequences for fruit development.

KW - cell separation

KW - cell wall

KW - Malus domestica

KW - pectin

KW - transcriptomic analysis

KW - transpiration

UR - http://www.scopus.com/inward/record.url?scp=85178414204&partnerID=8YFLogxK

U2 - 10.1111/tpj.16571

DO - 10.1111/tpj.16571

M3 - Article

AN - SCOPUS:85178414204

VL - 117

SP - 1413

EP - 1431

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 5

ER -